Metallic nanoparticles: microbial synthesis and unique properties for biotechnological applications,...

http://informahealthcare.com/btyISSN: 0738-8551 (print), 1549-7801 (electronic)

Crit Rev Biotechnol, Early Online: 1–15! 2013 Informa Healthcare USA, Inc. DOI: 10.3109/07388551.2013.819484

REVIEW ARTICLE

Metallic nanoparticles: microbial synthesis and unique properties forbiotechnological applications, bioavailability and biotransformation

Luciana Pereira1, Farrakh Mehboob2, Alfons J. M. Stams1,3, Manuel M. Mota1, Huub H. M. Rijnaarts4, andM. Madalena Alves1

1Institute for Biotechnology and Bioengineering, Centre of Biological Engineering, University of Minho, Campus de Gualtar, Braga, Portugal,2Ecototoxicology Research Programme, NIB, NARC, Park Road, Islamabad, Pakistan, 3Laboratory of Microbiology, Wageningen University,

Wageningen, The Netherlands, and 4Subdepartment of Environmental Technology, Wageningen University, Wageningen, The Netherlands

Abstract

The impact of nanotechnology in all areas of science and technology is evident. The expandingavailability of a variety of nanostructures with properties in the nanometer size range hassparked widespread interest in their use in biotechnological systems, including the field ofenvironmental remediation. Nanomaterials can be used as catalysts, adsorbents, membranes,water disinfectants and additives to increase catalytic activity and capability due to their highspecific surface areas and nanosize effects. Thus, nanomaterials appear promising for neweffective environmental technologies. Definitely, nanotechnology applications for site remedi-ation and wastewater treatment are currently in research and development stages, and newinnovations are underway. The synthesis of metallic nanoparticles has been intensivelydeveloped not only due to its fundamental scientific interest but also for many technologicalapplications. The use of microorganisms in the synthesis of nanoparticles is a relatively neweco-friendly and promising area of research with considerable potential for expansion. On theother hand, chemical synthesis occurs generally under extreme conditions (e.g. pH, tempera-ture) and also chemicals used may have associated environmental and human health impacts.This review is an overview of current research worldwide on the use of microorganisms duringthe biosynthesis of metallic nanoparticles and their unique properties that make them goodcandidates for many applications, including in biotechnology.

Keywords

Bioavailability of nanoparticles, biocatalysis,biosynthesis of nanoparticles,environmental biotechnology, metallicnanomaterials

History

Received 27 April 2012Revised 10 May 2013Accepted 15 May 2013Published online 7 August 2013

Introduction

In recent years, numerous types of metallic particles of

nanometer and micrometer dimensions (MNPs), and compos-

ites of these materials, have become key components in

different areas like catalysis (Ansari et al., 2009; Shan et al.,

2003, 2005a,b; Windt et al., 2005), environmental remediation

(Hennebel et al., 2009; Lukhele et al., 2010; Sharma et al.,

2008; Shin & Cha, 2008; Wang & Zhang, 1997; Xiu et al.,

2010), gene therapy (Andreu et al., 2008; Ewert et al., 2006;

Guihua et al., 2009; Patnaik et al., 2010), drug delivery (Akin

et al., 2007; Kubo et al., 2000; Rawat et al., 2006; Yellen et al.,

2005), imaging (Anceno et al., 2010; Lee et al., 2006,

2007; Lim et al., 2009), biomarkers (Ranzoni et al., 2012;

Xie et al., 2010), sensors (Fan et al., 2010; Li et al.,

2009; Xu et al., 2012) and energy (Che et al., 1998;

Ryu et al., 2010).

Among the vast number of unique properties of MNPs

(e.g. high surface area and magnetism), additional interest

relays on their high chemical activity (Akbarzadeh et al.,

2012; Bregar, 2004; Chirita & Grozescu, 2009; He & Zhao,

2005; Lee & Sedlak, 2008; Moores & Goettmann, 2006).

Control of nanoparticle size, shape and dispersity is the key to

selective and enhanced activity of MNPs (He & Zhao, 2007;

Tao et al., 2008).

With recent advances in nanotechnology and microbiol-

ogy, and due to efforts by different research groups to

synthesize, chemical and biologically, various types of metal

and metal oxide nanoparticles, novel materials have been

emerged (Bar et al., 2009; Chen & Gao, 2007; Jain et al.,

2010; Ma et al., 2004; Shahverdi et al., 2007; Yee et al.,

1999). Easy synthesis in a wide range of sizes and shapes,

facile surface conjugation to a variety of chemical and

biomolecular ligands, biocompatibility and high chemical and

photostability is possible (Chen & Gao, 2007; Evanoff &

Chumanov, 2004; Jain et al., 2008; Koebel et al., 2008).

Examples of metal nanoparticles include zerovalent iron, iron

oxide, silver, gold, copper, cobalt, platinum, manganese and

nickel nanoparticles and ferrites of the type MFe2O4 (M, a

divalent metal cation such as Mn2þ, Cu2þ, Co2þ or Ni2þ).

Nowadays, several types of iron nanoparticles are available on

the market, such as ferumoxtran, ferumoxsil, Resovist,

Address for correspondence: M. Madalena Alves, Institute forBiotechnology and Bioengineering, Centre of Biological Engineering,University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal.E-mail: [email protected]

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Feridex/Endorem, Gastromark/Lumirem, Sinerem and dif-

ferent iron oxides (Wagner et al., 2006; Wung & Jacobs,

1995). Studies show that nanoscale iron has a surface

area of 33.5 m2 g�1, whereas commercially available iron

powder has a surface area of only 0.9 m2 g�1 (Wang & Zhang,

1997). Reactions of zero-valent iron occur when iron corrodes

in the presence of water to form ferric or ferrous iron and

hydrogen:

Anaerobiccorrosion: Fe0þ 2H2O! Fe2þ þH2þ 2OH�

Aerobiccorrosion: 2Fe0þ O2þ 2H2O! 2Fe2þ þ 4OH�

2Fe2þ þ 0:5O2þH2O! 2Fe3þ þ 2OH�

Direct electron transfer from metallic iron to contaminants

has been recognized as an important pathway of contaminant

transformation by Fe0 in the subsurface, or indirect reductive

(bio)conversion by produced hydrogen serving as a secondary

electron donor (Lee et al., 2008; Liskowitz et al., 2009;

Noubactep, 2010; Reddy, 2010).

In this review, an overview of microbial synthesis of

metallic nanomaterials and the unique properties for many

applications is provided.

Microbial synthesis of metallic nanoparticles

A number of methods have been published for the chemical

synthesis of metallic nanoparticles. Many of them require

high temperatures and pressures (Eltzholtz & Iversen, 2011;

Harada et al., 2005; Marre et al., 2009; Ueji et al., 2008).

An alternative approach is the use of microorganisms for the

biological synthesis which occurs at ambient temperature and

pressure and at neutral pH. In nature, some nanomaterials are

synthesized by biological processes, such as intracellular

magnetite or greigite nanocrystallites by magnetotactic bac-

teria (Blakemore 1975, 1982; Mann et al. 1990), demonstrat-

ing the possibility of using microorganisms for the synthesis

of nanoparticles. Microorganisms are capable of adsorbing

and accumulating metals. They also secrete large amounts of

enzymes, which are involved in the enzymatic reduction of

metals ions (Huang et al., 1990; Rai & Duran, 2011; Zhang

et al., 2011). Microbial synthesis of nanoparticles can

take place either outside or inside the cell. Nanoparticles

can be divided into metallic nanoparticles and compound

nanoparticles.

Single metal nanoparticles

As shown in Supplementary Table 1, many different types

of bacteria have the ability to synthesize single metal

nanoparticles of different sizes and shapes. Emphasis has

been given on the synthesis of silver (Ag), gold (Au) and

palladium (Pd) nanoparticles. However, copper (Cu),

platinum (Pt), tellerium (Te) and titanium (Ti) nanoparticles

have also been synthesized (Baesman et al. 2007; Konishi

et al., 2007a; Prasad et al., 2007; Ramanathan et al., 2013).

Phylogenetically diverse bacteria are involved in the forma-

tion of nanoparticles. Pseudomonas, Lactobacillus, Bacillus

and sulfate-reducing bacteria are the important microbial

catalysts for the synthesis of different nanoparticles. Most

of the bacteria synthesize nanoparticles extracellularly.

Consequently, no additional steps for extraction are needed.

Most of the nanoparticles reported are spherical, but some

have different shapes, such as ultrathin platelets and octahe-

dral platelets (Lengke et al., 2006a), cubic (Jain et al., 2010),

nanorods and nanoprisms (Deplanche & Macaskie, 2008) and

equatorial triangles (Klaus et al., 1999; Konishi et al., 2007b).

Carbonyl group-containing compounds (aldehyde/ketones)

are suggested to have a role in triangle nanoparticle formation

(Konishi et al., 2007b). Chloride and cyanide groups were

found to be dominant on the surface of octahederal platelets

(Lengke et al., 2006a).

Though nanoparticles formed by different microorganisms

have different dispersity, most of them are fairly mono-

dispersed. Furthermore, biologically formed Ag nanoparticles

are stable and do not aggregate up to six months (Fu et al.,

2006; Namsivayam et al., 2010). However, tellurium

nanoparticles aggregate easily and form a larger complex

(Baesman et al., 2007).

Compound nanoparticles

Compound nanoparticles consist of either sulfides or oxides

of various metals (Supplementary Table 1). Sulfide nanopar-

ticles are generally formed at low redox potential in anoxic

conditions, while oxide nanoparticles are formed at higher

redox potential in oxic and anoxic conditions. Just like the

metallic nanoparticles, phylogenetically diverse bacteria

have the ability to synthesize the compound nanoparticles

(e.g. Rhodobacter, Klebsiella, Lactobacillus and sulfate-

reducing bacteria).

Heavy metals like lead (Pb), cadmium (Cd), zinc (Zn) and

mercury (Hg) are pollutants and can be remediated by

forming the metal-sulfide nanoparticles. Likewise, radio-

nucleide pollutants like mobile hexavalent uranium, U(VI),

are precipitated as nanoparticles of tetravalent uranium by

Desulfosporosinus sp. (Suzuki et al., 2002) and Shewanella

oneidensis (Marshall et al., 2006). Shewanella oneidensis is

also capable of reducing technetium (VII) into Tc(IV)

(Marshall et al., 2008).

Neutophilic iron oxidizing bacteria like Leptothrix,

Gallionella, Mariprofundus form extracellular iron oxide

nanoparticles (Chan et al., 2011; Hashimoto et al., 2007;

Suzuki et al. 2011). Exopolysaccharides act as templates for

iron oxide nucleations in these bacteria (Chan et al. 2004).

Iron-reducing bacteria like Geobacter bemidjiensis tend to

accumulate ferric oxyhydroxide nanoparticle aggregates that

are suggested to support their planktonic growth (Luef et al.,

2013). Magnetosomes are perhaps the most extensively

studied nanoparticles and are worthy of a separate subject

of study. They are specialized organelles for navigation in

magnetotactic bacteria and consist of a nanosized magnetic

iron crystal surrounded by a membrane (Jogler & Schuler,

2009). Magnetosomes contain crystals of iron oxide,

i.e. magnetite (Fe3O4) or iron sulfide such as greigite

(Fe3S4). The same group of magnetotactic bacteria synthe-

sizes both magnetite and greigite (Moskowitz et al. 2008).

Non-magnetic minerals such as iron pyrite (FeS2), mack-

inawite (tetragonal FeS) and sphalerite (cubic FeS), were also

found in magnetosomes (Mann et al., 1990; Posfai et al.,

1998). Non-magnetotactic bacteria can also produce magnet-

ite (Lovley et al., 1987). Magnetosomes are intracellular but

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there are reports that describe extracellular formation of

magnetite (Bharde et al., 2005; Lovley, 1987; Zhang et al.,

1998) and magnetic iron sulfide (Sakaguchi et al., 1993).

Generally, magnetosomes are considered to be of high

chemical purity but certain contaminants have been found

(Bazylinski, 1993; Towe & Moenich, 1981) which led to the

idea of doping of magnetosomes with various metals to

change properties (Roh et al., 2001; Staniland et al., 2008).

This could be useful in the potential development of

nanosized materials with different properties.

Transition metals (Cr, Mn, Co, Ni and Zn) and lanthanide

(Nd, Gd, Tb, Ho and Er) substituted magnetites were

synthesized by thermophilic Thermoanaerobacter ethanolicus

(TOR-39) or by psychrotolerant Shewanella sp. strain PV-4

(Moon et al., 2007). Bacterially synthesized Mn- and Zn-

substituted magnetites had higher magnetic susceptibility and

saturation magnetization than pure biomagnetite while lan-

thanide substituted magnetites have less saturation magnet-

ization (Moon et al., 2007).

Three strains of magnetotactic bacteria, Magnetospirillum

gryphiswaldense (MSR-1), Magnetospirillum magnetotacti-

cum (MS-1) and Magnetospirillum magneticum (AMB-1)

were able to incorporate 0.2 to 1.4% of cobalt in magnetite

which led to an increase of 36–45% in coercive field of

magnetosomes, i.e. field necessary to reverse their magnet-

ization (Staniland et al., 2008). Cobalt doped magnetite

particles are potentially useful in carrying out magnetic

hyperthermia for cancer therapy. An increase in the heating

efficiency of the extracted chains of cobalt doped magneto-

somes extracted from AMB-1 was observed which could

be useful for the therapy (Alphandery et al., 2011). The

Fe(III)-reducing bacterium Geobacter sulfurreducens was

used to synthesize cobalt ferrite (CoFe2O4) nanoparticles

with low temperature coercivity and an effective anisotropy

constant (Coker et al., 2013).

Factors affecting microbial synthesis ofmetallic nanoparticles

Microbial nanoparticle synthesis is directly affected by incu-

bation conditions, such as redox conditions (Baesman et al.,

2007; Deplanche & Macaskie, 2008; Gauthier et al., 2010;

Kashefi et al., 2001; Konishi et al., 2007a; Lloyd et al., 1999;

Marshall et al., 2008; Prakash et al., 2010; Tanaka et al., 2010),

temperature (Gurunathan et al., 2009; Juibari et al., 2011;

Lengke et al., 2006a, 2007), pH (Deplanche & Macaskie,

2008; He et al., 2007; Konishi et al., 2007b; Sinha & Khare,

2011), mixing (Mokhtari et al., 2009), irradiation (Mokhtari

et al., 2009; Saifuddin et al., 2009), incubation time (Bai et al.,

2006; Ogi et al., 2010; Sinha & Khare, 2011; Wen et al., 2009),

nature (Lengke et al., 2006a; Mokhtari et al., 2009; Zhang

et al., 2005) and concentration (Feng et al., 2007; Gurunathan

et al., 2009; He et al., 2008; Juibari et al., 2011; Lengke et al.,

2006b; Parikh et al., 2008) of the parent compound or metal

species, and colloidal interaction conditions, that control the

size, shape, localization and dispersity of the nanoparticles

formed. In particular, redox conditions, i.e. oxic or anoxic

conditions are of importance.

All the Ag nanoparticles reported are formed aerobically

(Bai et al., 2011; Fu et al., 2006; Kannan et al., 2011;

Kalimuthu et al., 2008; Prakash et al., 2010; Sintubin et al.,

2009; Zhang et al. 2005), but Au particles are formed both

aerobically (Ahmad et al., 2003c; Nair & Pardeep, 2002;

Nangia et al., 2009) and anaerobically (Deplanche &

Macaskie, 2008; Kashefi et al., 2001; Konishi et al.,

2007b). Except for Bacillus sphaericus (Creamer et al.,

2007) and Shewanella oneidensis (De Windt et al., 2005), all

the Pd nanoparticles are synthesized anaerobically (Baxter-

Plant et al., 2003; Bunge et al., 2010; Chidambaram et al.,

2010; Deplanche et al., 2010; Gauthier et al., 2010; Hennebel

et al., 2011; Humphries & Macaskie, 2005; Lloyd et al., 1999;

Mikheenko et al., 2008; Redwood et al., 2008; Yong et al.,

2002). Platinum (Pt) (Konishi et al., 2007a), technetium (Tc)

(Marshall et al., 2008) and tellurium (Te) (Baesman et al.,

2007) particles have been synthesized anaerobically except

for microaerobic synthesis of Te by Magnetospirillum

magneticum AMB-1 (Tanaka et al., 2010). Though magneto-

somes are generally formed in microaerobic conditions, there

are reports of the formation of magnetite in fully aerobic

(Bharde et al., 2005) and anaerobic (Bazylinski et al., 1988;

Lovley, 1987) conditions. During Au nanoparticle formation

by Acinetobacter species, the rate of gold ion reduction is

drastically enhanced in the absence of oxygen (Bharde et al.,

2007).

Bacterial synthesis of nanoparticles is enhanced at higher

temperature (Juibari et al., 2011), below the optimal tem-

perature for the microbial species and reactions involved. The

size of the Au and Pd nanoparticles formed by cyanobacter-

ium Plectonema boryanum slightly increased with an increase

in temperature (Lengke et al., 2006a, 2007). In contrast, in

E. coli, increasing the temperature up to 60 �C not only

increased the rate of Ag nanoparticle synthesis but also led to

a smaller size of the particles. This was attributed to the

increased activity of the enzyme responsible for the synthesis

of nanoparticles (Gurunathan et al., 2009).

pH is an important factor and depends on the microorgan-

ism, type of nanoparticle and the culture conditions of

biosynthesis. Gold nanoparticles of 10–20 nm were formed at

pH 7 by Shewanella algae, while large nanoparticles with

variable size were obtained at lower pH (He et al., 2007;

Konishi et al., 2007b). By contrast, the size of gold

nanoparticles formed by E. coli and D. desulfuricans was

smaller at acidic pH as compared with neutral or alkaline

conditions (Deplanche & Macaskie, 2008). Monodispersed

and spherical mercury nanoparticles were formed by

Enterobacter at pH 7, while particles of irregular shape and

size were formed at pH 6 and higher numbers of extremely

smaller particles were found at higher pH (Sinha & Khare,

2011). In E. coli, the highest number of Ag nanoparticles,

with the fastest rate of formation, was found at pH 10

(Gurunathan et al., 2009).

Generally, the size of nanoparticles increases with the

length of reaction/incubation time, as found by Bai et al.

(2006, 2009a) for the formation of ZnS and CdS nanoparticles

by Rhodopseudomonas palustris and Rhodobacter sphaer-

oides. The increase in the diameter was attributed to

nucleation effects where small particles agglomerate to form

large multimers (Holmes et al., 1997). By increasing the

reaction time, B. megaterium formed less spherical particles

and the particles increased in size and came out of the cell

DOI: 10.3109/07388551.2013.819484 Metallic nanoparticles 3

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(Wen et al., 2009). Cell free extract of Shewanella algae also

yielded larger particles with extended incubation time (Ogi

et al., 2010). Longer incubation times of cell suspensions of

an Enterobacter sp. resulted in a larger number of spherical

Hg nanoparticles dispersed uniformly (Sinha & Khare, 2011).

The growth and stationary phases were found best for fast

synthesis of a maximum number of nanoparticles with higher

stability. During CdS synthesis, E. coli synthesized 20-fold

more nanoparticles during stationary than at the late loga-

rithmic phase (Sweeney et al., 2004). Ag nanoparticles by

B. licheniformis were more abundant and stable during the

stationary phase (Kalimathu et al., 2008). Similar results were

obtained for the synthesis of Ag nanoparticles by E. coli

(Gurunathan et al., 2009).

The culture supernatant of K. pneumonia yielded smaller

size nanoparticles when shortly pre-mixed (300 rpm for

5 min) in the dark and then irradiated with an effective dose

of visible light (1000mmol m�2 s�1) (Mokhtari et al., 2009).

Microwave irradiation also resulted in rapid synthesis of Ag

nanoparticles from the culture supernatant of B. subtilis

(Saifuddin et al., 2009). Hence, irradiation has been found to

reduce the size and increase the rate of nanoparticle

formation.

The parent compound used for the synthesis of nanopar-

ticles also affects the size of the nanoparticles.

Corynebacterium strain SH09 formed Ag nanoparticles only

by reducing the diamine silver complex, while no bioreduc-

tion of silver nitrate occurred (Zhang et al., 2005). In the

cyanobacterium Plectonema boryanum, the addition of

Au S2O3ð Þ3�2 produced cubic gold nanoparticles associated

with membrane vesicles, while with AuCl�4 as the starting

compound, ultrathin octahederal platelets gold nanoparticle

are formed only inside the cell (Lengke et al., 2006a). The use

of AgCl2 led to the formation of nanoparticles with different

shapes and wider size range distribution than AgNO3

(Mokhtari et al., 2009).

Starting ion concentrations seemed to have a more

pronounced effect on the size of nanoparticles than the

temperature (Juibari et al., 2011). The size of the metallic

gold nanoparticles, formed by cyanobacteria, increased with

increasing gold concentrations (Lengke et al., 2006b). At a

lower concentration of gold, spherical nanoparticles were

produced while at higher concentration nanowires with a

network structure were produced (He et al., 2008). During the

synthesis of gold nanoparticles by Rhodobacter capsulatus,

higher concentrations of AuCl�4 resulted in higher numbers

and a larger size of particles (Feng et al., 2007). By contrast,

in other studies, the size of Ag nanoparticles decrease with

increasing concentrations up to 5 mM silver nitrate, while at

that concentration the largest number of nanoparticles was

found (Gurunathan et al., 2009; Parikh et al., 2008).

Ureibacillus thermosphaericus produced Ag nanoparticles

with silver ion concentrations of up to 10 mM, but bulk size

particles were formed when the concentration was 100 mM

(Juibari et al., 2011).

Nanoparticles are subjected to attractive van der Waals

interactions and to electrostatic double layer interactions,

which are generally repulsive when surfaces are either

negatively or positively charged, and described by the

Derjaguin, Landau, Verwey, and Overbeek (DLVO)

theory (Derjaguin & Landau, 1945, 1993; Overbeek, 1999).

In addition, steric interactions (repulsive or attractive) need to

be added to that when organic molecules adsorb onto these

particles. Particles are stable in suspension when the repulsive

forces dominate, which is generally at sufficiently low ionic

strength and/or by additional steric interactions (Rijnaarts

et al., 1999). Cell–nanoparticle interactions are also con-

trolled by these colloidal mechanisms (Jucker et al., 1998).

In many systems, colloidal interactions are attractive leading

to nanoparticles incorporation into larger particles. These can

either remain suspended or flocculate, depending on the size

of the particles formed. Higher and larger particle yields,

could therefore, at least partly, be the result of increased

colloidal interaction. The yield of gold nanoparticles by cell

extracts of S. algae was found to be 4-fold higher than by the

resting cells (Ogi et al., 2010). Addition of an effective

capping agent like alkanethiols restricts the size of nanopar-

ticles. The addition of dodecanethiol results in small sizes

(52.5 nm), keeps the spherical shape and promotes the

monodispersity during the formation of gold particles by

B. megaterium (Wen et al., 2009).

The modulation of different factors that affect

nanoparticle biosynthesis can be brought about, not only to

get the monodispersed nanoparticles with small uniform size

but also to change the localization so that they can be easily

extracted.

Mechanism of microbial synthesis of metallicnanoparticles

MNP synthesis by bacteria

While considerable literature is available on the bacterial

biosynthesis of nanoparticles, the mechanisms are not yet

fully understood. The main reasons for bacteria producing

nanoparticles are chemolithotropic growth, use of metal ions

for specific function, e.g. synthesis of magnetosomes or

terminal electron acceptors and detoxification mechanisms

(Krumov et al., 2009). The mechanism of formation of

magnetosomes has been studied and reviewed in detail by

Bazylinski & Frankel (2004) and Jogler & Schuler (2009) and

is a separate subject of discussion which is beyond the scope

of this review.

Since metal ions have a positive charge and the cell wall a

negative due carboxylate and other groups, metal-ions

accumulate in the diffusive part of the electrical double

layer (Rijnaarts et al., 1995a,b) and can easily be deposited

into the cell surface matrix via the electrostatic interaction at

the molecular level, by simple ionic binding or by bridging

polymeric structures (Mukherjee et al., 2002; Neal, 2008).

Various metals can enter the cell via specific transporters as

analogues of essential chemicals, e.g. cadmium may be

transported via energy dependent special transporters for

magnesium/manganese (Cunnigham & Lundie, 1993; Holmes

et al., 1997).

For metal nanoparticle synthesis, it is essential that

bacteria overcome the toxicity of metals by binding them

with various groups and proteins. Different metal binding

proteins are secreted by bacteria (Lengke et al., 2007; Nair &

Pardeep, 2002). The 2-fold increase in the protein content of

Clostridium thermoaceticum during the precipitation of Cd,


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was attributed to an extracellular Cd-binding protein

(Cunnigham & Lundie, 1993). Apart from metal binding

proteins, cyanobacterial polysaccharides have many uronic

acid subunits which through the carboxylic groups bind

metals (Lengke et al., 2007). A periplasmic silver binding

protein silE was formed during the formation of Ag

nanoparticles by a Morganella sp. (Parikh et al., 2008).

Once inside the cell, the metals can be reduced either

fortuitously or in a specific metabolic process. For example,

formation of Au nanoparticles by sulfate reducing bacterial

enrichment is associated with a metabolic process. These

bacteria produce H2S, which results in the formation of metal

sulfides (Lengke & Southam, 2006). Bacillus selenitireducens

and Sulfurospirillum barnesii synthesized the Te nanoparticle

via the dissimilatory reduction of Te(VI) or Te(IV) (Baesman

et al., 2007). Plectonema boryanum formed nanoparticles by

reduction of both gold(I) thiosulfate and gold(III) chloride

complexes (Lengke et al., 2006a). Gold(I) sulfide is formed as

intermediate during the synthesis of gold(III) chloride by

cyanobacteria. Presumably either the released sulfur (S) from

cysteine or methionine or S from dying bacteria bound with

the gold to form gold(I) sulfide (Lengke et al., 2006a,b).

Similarly, insoluble AgCl was the main intermediate in the

synthesis of Ag nanoparticles from AgNO3 by K. pneumonia

(Mokhtari et al., 2009).

MNP synthesis in fungi

Several species of fungi, including yeasts, have been reported

to synthesize metallic nanoparticles. Cadmium sulfide crys-

tallites synthesized by Candida glabrata was reported by

Cameron et al. (1989). Kowshik and coworkers (2002)

reported the intracellular synthesis of cadmium sulfide

nanoparticles by the fission yeast Schizosaccharomyces

pombe. Furthermore, Krumov et al. (2007) used a fed-batch

bio-process to cultivate both C. glabrata and S. pombe in the

presence of cadmium levels up to 100 mg L�1 and showed

that cadmium is not excreted or precipitated by the cell, but

immobilized by an intracellular detoxification mechanism.

Silver nanoparticles have been synthesized by many fungi,

namely, Phanerochate chrysosporium (Vigneshwaran et al.,

2006), Phoma glomerata (Birla et al., 2009), Trichoderma

reesei (Vhabi et al., 2011) Aspergillus fumigatus (Bhainsa

et al., 2006), Aspergillus niger (Gade et al., 2008), Fusarium

solani (Ingle et al., 2009) and Fusarium oxysporum (Ahmad

et al., 2003a). The latter fungus is also involved in gold

(Mukherjee et al., 2002) and platinum nanoparticles (Riddin

et al., 2006). A research group was successful in synthesizing

zirconia nanoparticles (Bansal et al., 2004). They also found

that F. oxysporum is a biological model system for the

extracellular bioleaching of hollow spherical silica nanopar-

ticles (Bansal et al., 2005a) as well as the synthesis of titania

nanoparticles (Bansal et al., 2005b). Size-controlled fungal

biosynthesis by a Penicillium species was reported by Zhang

et al. (2009). The extracellular fungal biosynthesis seems to

involve extracellular reductases coupled to capping proteins.

Duran et al. (2005) found that aqueous silver ions,

when exposed to several Fusarium oxysporum strains, are

reduced in solution, thereby leading to the formation of

silver hydrosol, forming silver 20–50 nm nanoparticles.

The reduction of the metal ions occurred by a nitrate-

dependent reductase and a shuttle quinone extracellular

process. The fungus Verticillium was reported to synthesize

gold nanoparticles (Mukherjee et al., 2001). This fungus was

also used to obtain very uniform CaCO3 nanocrystallites in

the range 70–100 nm (Rautaray et al., 2004). Both

Verticillium and Fusarium could synthesize extracellular

magnetic nanoparticles (Bharde et al., 2006). Interestingly,

very few publications reporting the biosynthesis of magnetic

nanoparticles (iron or cobalt) by fungi are available.

The role of enzymes in the microbial synthesis of metallic

nanoparticles

Microbial synthesis of nanoparticles is generally associated

with an enzymatic process. The cystein desulfhydrase activity

(resulting in formation of sulfide from cysteine) is thought to

be responsible for the CdS and PbS nanoparticle formation by

Rhodopseudomonas palustris and Rhodobacter sphaeroides

respectively (Bai et al., 2009a; 2009b; Bai and Zhang, 2009).

Though glutathione may affect the process, no correlation was

observed between the amount of glutathione and the synthesis

of nanoparticles (Sweeney et al., 2004). The higher rate of Ag

nanoparticle synthesis by E. coli in the medium containing

nitrate was attributed to the activity of nitrate reductase/

nitroreductase (Gurunathan et al., 2009). The culture super-

natant of B. subtilis showed nitrate reductase activity, hence

leading to the conclusion that nitrate reductase together with

some electron shuttling compound may be involved in the Ag

nanoparticle synthesis (Saifuddin et al., 2009). The formation

of Ag nanoparticles in Pseudomonas aeruginosa was

attributed to nitrate reductase and the capping was supposed

to be due to rhamnolipids formation (Kumar & Mamidyala,

2011). Piperitone, which is an inhibitor of nitroreductase can

partially inhibit the reduction of Agþ ions by Enterobacteria

sp. (Shahverdi et al., 2007). The nitroreductase is believed to

be involved in metal reduction together with photosensitive

electron shuttles (Mokhtari, 2009). Shewanella algae reduced

Au(III) with H2 but not with lactate. Hence the involvement of

a hydrogenase in the reduction was suggested (Kashefi et al.,

2001). Probably the periplasmic hydrogenase catalyzed the

oxidation of hydrogen and released electrons that are taken up

by Au(III) which is reduced to Au(0) (Kashefi et al., 2001).

The synthesis of Pt nanoparticles by Shewanella algae occurs

by a different mechanism than Au nanoparticle synthesis, as

in this case lactate can act as an electron donor (Konishi et al.,

2007a). During the formation of Pd nanoparticles by

Shewanella onediensis, a periplasmic hydrogenase is likely

involved to precipitate Pd on cells which can later on become

self-sustainable by the ability of crystalline solid Pd(0) to

absorb H2 and autocatalytically reduce more Pd(II) (De Windt

et al., 2005). Cu(II), a known inhibitor of periplasmic

hydrogenases partially inhibited the Au(III) reduction process

in E. coli and D. desulfuricans, showing the involvement of

hydrogenases, but also indicating the existence of other

mechanisms of Au(III) reduction (Deplanche & Macaskie,

2008). In Shewanella oneidensis MR-1, two hydrogenases

were directly involved in technetium(VII) reduction, the NiFe

hydrogenase had a higher Tc reduction activity than the

Fe-only hydrogenase (Marshal et al., 2008).


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A membrane bound oxido-reductase is proposed to play an

important role in the synthesis of Ag, Cu2O and TiO2 by

Lactobacillus sp. Its activity is modulated by the pH and

redox potential (Jha et al., 2009; Prasad et al., 2010).

Purified enzymes have also been tested. Kumar et al.

(2007a) used the NADPH-dependent nitrate reductase

purified from the fungus Fusarium oxysporium for the

synthesis of the Ag nanoparticles. The NADPH-dependent

sulfite reductase from the same organism catalyzed the

synthesis of Au nanoparticles (Kumar et al., 2007b).

However, none of the purified enzymes was checked for

the synthesis of other metal nanoparticles. Acinetobacter

species were found to synthesize the Au nanoparticles in the

presence of bovine serum albumin (BSA) protein (Bharde

et al., 2007). Addition of BSA induced the expression

of genes that code for a protease having a role in the

formation of nanoparticles. Subsequent experiments showed

nanoparticle synthesis by applying a commercial protease.

Pepstatin, a known inhibitor of protease, inhibited

the formation of Au nanoparticles (Bharde et al., 2007).

Recently, a fibrinolytic enzyme URAK purified from Bacillus

cereus NK1 was used to synthesize both the Au and Ag

nanoparticles. The enzyme was found to be immobilized on

the nanoparticles, which is advantageous for application of

enzyme (Deepak et al., 2011).

Pure a-amylase was capable of forming Au nanoparticles.

The activity of the enzyme was retained when complexed

with the nanoparticle. It was proposed that the two free and

exposed thiol groups (-SH) in the side chains of cysteine can

act as reducing agents to reduce gold chloride to Au

nanoparticles. It was further found that another enzyme

EcoR1 with an exposed thiol group can form the Au

nanoparticles contrarily to enzymes without thiol groups

(ribonuclease A, lysozyme, horse radish peroxidase etc.) or

enzymes with embedded thiol groups (BSA). The modifica-

tion of the thiol group led to the inability of the enzyme

to form the Au nanoparticles (Rangnekar et al., 2007).

When AgNO3 was added to BSA solution, silver nanoparti-

cles were quickly formed, but no synthesis of Au nanopar-

ticles was observed upon addition of HAuCl4 in BSA.

However, when both the AgNO3 and HAuCl4 were concomi-

tantly added into the BSA solution both Ag and Au

nanoparticles are formed. It was supposed that BSA first

reduces the silver ions to the Ag metal which in turn is

oxidized to reduce the gold ions to Au nanoparticles. The

reduction was attributed to tryptophan residues of the BSA

(Murawala et al., 2009). Pure amino acids like aspartate for

the production of Au nanoparticles (Mandal et al., 2002) and

tyrosine under alkaline conditions for the synthesis of Ag

nanoparticles have also been used (Selvakannan et al., 2004).

Under the alkaline conditions the phenolic groups of tyrosine

are ionized which enables the reduction of silver ions

(Selvakannan et al., 2004). Purified rhamanolipids from

P. aeruginosa were also used to synthesize the Ag

nanoparticles (Kumar et al., 2010).

Enzymes probably transfer the electrons through the cyto-

chromes to reduce the metal ions. Through studies with

deletion mutants and purified cytochromes it was demon-

strated that the outer-membrane (OM) decaheme cytochrome

(MtrC) of Shewanella oneidensis is responsible for the

transfer of electrons to U(VI) to form the extracellular UO2

nanoparticles (Marshal et al., 2006). In Shewenella oneiden-

sis, the deletion of two hydrogenases did not completely

eliminate the ability to reduce technetium (VII). However,

mutants lacking the outer membrane c-type cytochromes

MtrC and OmcA were not efficient in reducing Tc(VII) to

nanoparticulate TcO2 � nH2O(s). Moreover, reduced MtrC and

OmcA were oxidized by Tc VIIð ÞO�4 , confirming the direct

electron transfer from the MtrC and OmcA to TcO�4 (Marshal

et al., 2008). In Shewanella oneidensis outer membrane

c-type cytochromes have been shown to affect the size and

activity of the extracellular nanoparticles. The mutant lacking

outer membrane c-type cytochromes exhibited decrease in

particle size and higher activity (Ng et al., 2013).

Stabilization of nanoparticles

Once synthesized, the nanoparticles can be stabilized

by different capping agents. Proteins are thought to stabilize

the nanoparticles by capping the Au nanoparticles (Ahmad

et al., 2003b; He et al., 2008). CdS nanocrystals formed by

E. coli were capped by polyphosphates (Sweeney et al.,

2004) and the Ag nanoparticles formed by P. aeruginosa

were capped by rhamanolipids (Kumar & Mamidyala,

2011). Experiments were conducted to see the differential

protein expression patterns. Proteins of 80–10 kDa are

believed to reduce chloraurate ions and to cap Au nanopar-

ticle in Thermonospora sp. (Ahmad et al., 2003b). In

another study, SDS-PAGE analysis identified five different

proteins of molecular mass between 14 and 98 kDa that may

reduce chloraurate ions and cap Au nanoparticle in

Rhodopseudomonas capsulata (He et al., 2008). Most of the

proteins are over-expressed as compared to control during the

synthesis of ferromagnetic Co3O4 by Brevibacterium casei.

The authors speculated that the over-expression is a stress

response of bacteria to the salt (Kumar et al., 2008).

Attempts were also made to identify the exact residues

bound with the nanoparticles in order to understand the

mechanism of synthesis. Alteration of carboxyl group

severely limited metal deposition at the cell wall, indicating

that carboxyl group is the major site of metal deposition

(Beveridge & Murray, 1980). Ionized carboxyl of amino acids

and the amide of the peptide chain were the main groups for

depositing silver diamine, and some reducing groups such as

aldehyde and ketone were involved in subsequent reduction

(Zhang et al., 2005). Bioreduction of Au S2O3ð Þ3�2 is sug-

gested through the interaction with P, S or N ligands of the

membrane vesicles as indicated by transmission electron

microscopy and energy-dispersive X-ray spectrometery

(TEM-EDS) (Lengke et al., 2006a). During the formation of

Ag nanoparticles by Morganella sp., the visibility of an amide

I and amide II band at the surface of Ag nanoparticles

suggested the involvement of Ag specific proteins (Parikh

et al., 2008). Amide I and amide II bands were also identified

on the surface of Au nanoparticles synthesized by

Rhodopseudomonas capsulata (He et al., 2008). Figure 1

illustrates the various steps involved in the formation of

nanoparticles.


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Unique properties of metallic nanoparticles

Nanoparticles have found application in many fields such as

of physics, electronics, energy, chemistry, biology, pharma-

ceuticals, cosmetics, medicine, the food industry, manufactur-

ing, analytical chemistry, engineering, automotive, energy,

agriculture, biological and environmental research and even

entertainment (Farre et al., 2009; Masciangioli and Zhang,

2003; Neal, 2008). Nanoparticle properties make them also

good candidates for biotechnological applications, namely on

bioremediation (Alvarez & Cervantes, 2011; Liu, 2006;

Tungittiplakorn et al., 2005). Sun et al. (2006) reported on

the synthesis of iron nanoparticles (dimensions �60 nm) that

function both as adsorbers and reductants of many compounds

(Figure 2). Ag nanoparticles applications include their use as

antimicrobial agents (Hennebel et al., 2009).

Magnetic properties

The application of magnetic particle technology to solve

environmental problems has received considerable attention

in recent years. As examples, ferrites were shown to exhibit

excellent adsorptive properties of pollutants such as dyes

(Qu et al., 2008; Wu et al., 2004; Wu and Qu, 2005; Zhang

et al., 2007a), arsenite (Zhang et al., 2007b) and phosphate

(Zhang et al., 2009) with the advantage of being recovered

from water by magnetic separation. Activated carbon has

been widely described as a good adsorbent material (Faria

et al., 2005, 2008; Malik, 2004), but suffers from the

disadvantage of difficult and expensive recovery and re-use.

Therefore, combining the advantages of carbon materials and

magnetic properties of nanoparticles in novel adsorbents,

opens promising possibilities in the field of adsorption

technology (Oliveira et al., 2002; Yang et al., 2008; Zhang

et al., 2007a). Bio-nanomaterials have also been synthesized,

leading to the formation of magnetically labelled cells, which

could be easily separated from the system using an

appropriate magnetic separator (Mosiniewicz et al., 2009).

Magnetic modification of microbial cells enables the prepar-

ation of smart biocomposites receptive to external magnetic

field. Magnetic nanoparticules, such as magnetic iron oxide,

attached on the surface of bacterial, algae and yeast cells have

been used as magnetically responsive biosorbents for removal

of water-soluble organic dyes and heavy metal ions

(Safarikova et al., 2005, 2008; Yavuz et al., 2006) and for

biocatalysis (Safarik & Safarikova, 2007; Safarikova et al.,

2009). Mosiniewick et al. (2009) have proposed an inexpen-

sive and simple procedure of magnetic adsorbents preparation

for removal of dyes. They have modified cells of the yeast

Kluyveromyces fragilis and the unicellular algae Chlorella

vulgaris by contact with water-based magnetic fluid

Figure 1. Proposed mechanism of formation of nanoparticles.

Figure 2. A core-shell structure for iron nanoparticles in aqueoussolution. The core is made of metallic iron while the shell consistsmostly of iron oxides and hydroxides. Iron nanoparticles exhibitcharacteristics of both iron oxides (e.g. as a sorbent) and metallic iron(e.g. as a reductant) (Sun et al. 2006).


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containing maghemite nanoparticles. Applications of mag-

netic microbial adsorbents for heavy metal ions and organic

xenobiotics removal are described in the report of Safarik &

Safarikova (2007).

Adsorption properties

In general, the conventional adsorbents are highly porous

particles in order to ensure adequate surface area for

adsorption. However, the existence of intraparticle diffusion

may lead to the decreases in the adsorption rate and available

capacity, particularly for macromolecules (Mak and Chen,

2004). Developing an adsorbent with large surface area and

small diffusion resistance has significant importance in

practical use. The situation led the researchers to develop

an absorbent which have large surface area and small

diffusion resistance. Nanostructured solids have gained

extreme interest due to their sorption, catalytic, magnetic,

optical and thermal properties. At nanoscale, materials show

high surface area and greater active sites for interaction with

other species (Hristovski et al., 2007; Khaleel et al., 1999;

Ling et al., 2006). Magnetic adsorbents can easily be

reclaimed and separated by magnetic fields. Application of

nanoadsorbents in the field of wastewater treatment is

becoming an interesting area of research. Currently, nanoma-

terials used as adsorbents are one of the best candidates for

dye removal (Faraji et al., 2010; Hashemian, 2010; Zhou

et al., 2010) and heavy metals (Chang & Chen, 2005a).

Numerous studies demonstrate that bulk iron oxides have

good efficiency to remove heavy metals from aqueous

solutions, nevertheless, due to high surface area nanoparticles

have better efficiency than bulk particles of same materials

(Ponder et al., 2001). The non-toxic and non-corrosive nature

is another benefit with these adsorbents (Sharma et al., 2009).

Many researchers have found that adsorption is highly

dependent on pH, temperature and ionic strength (Sharma

et al., 2009; Chang & Chen, 2005a,b; Sun et al., 2011). The

surface state of nanoparticles also seems to be a crucial factor

for adsorption. (Ko et al., 2007). The surfaces of nanoparticles

are often modified by capping agents such as polymers,

inorganic metals or oxides, and surfactants to make them

stable, biocompatible, and suitable for further functionaliza-

tions and applications (Bukat et al., 2003; Sun et al. 2011).

Organic/inorganic compounds bound to surfaces, induce the

nanoparticle surface with a positive/negative charge at

different pH conditions. Polymer coated surfaces possessing

large surface area and surface properties, such as hydropho-

bicity or hydrophilicity, can be controlled under different

conditions of temperature, pH, and ionic strength. Affinity

ligands connected surfaces, such as Cu2þ and other metal

ions, have the advantage of low cost and high stability and can

be used for affinity adsorption and separations.

Immobilizing agent of microorganisms and enzymes

Magnetic particles are applied to immobilize enzymes and

other bioactive agents in analytical biochemistry, medicine

and biotechnology (Koneracka et al., 2006). Enzymes can be

stabilized in the form of single-enzyme nanoparticles (SENs)

which results an extended lifetime of the biocatalyst. The first

SENs were assembled by Kim & Grate (2005) using

chymotrypsin as a model enzyme. Liu et al. (2004), reported

the synthesis of magnetic silica nanospheres with the core-

shell structure of magnetite (Fe3O4)/silica and their use for

protein immobilization. Yang et al. (2004), have entrapped

horseradish peroxidase (HRP) in magnetite containing spher-

ical silica nanoparticles. Although the catalytic activity of

entrapped HRP, towards the substrate 2,20-azino-bis(3-ethyl-

benzothiazoline-6-sulfonic acid (ABTS), was slightly lower

than that of free HRP, kcat of 82.5 and 106 s�1, respectively,

the entrapped enzyme had a higher temperature tolerance and

a higher stability. Moreover, since magnetic catalysts are

separated from the solution by magnetic separation, the

enzyme entrapped catalyst could be easily recovered from the

reaction mixture by simple removal of the supernatant and

could be further applied, maintaining 81% of activity after

five cycles. Tsang et al. (2006) have synthesized and

characterized silica-encapsulated iron oxide magnetic nano-

particles of controlled dimension as an enzyme carrier. They

showed that the relatively smaller sized silica-coated mag-

netic nanoparticles could carry the enzyme b-lactamase via

chemical linkages on the silica overlayer, without blocking the

active centre of the enzymes (which often encountered with

conventional solid supports). The recovery and reusability of

the nanoparticle-supported enzymes upon application of

magnetic separation was also demonstrated in this study.

Immobilized microbial cells are frequently used in

bioconversions, biotransformation and biosynthesis processes

due to their better operational stability, easier separation from

products for possible reuse and satisfactory efficiency in

catalysis compared to free cells. Cells of Pseudomonas

delafieldii, immobilized in magnetic polyvinyl alcohol (PVA)

beads, could be easily collected or separated magnetically

from a biodesulfurization reactor (Shan et al., 2003). Complex

cell nanomaterials are generated by entrapment or adsorbing

nanoparticles onto the surfaces of microbial cells, which

increase the reaction activity of original cells and reduce

environmental pollution. Adsorption is perhaps the simplest

of all the immobilization techniques without mass transfer

problems. A new technique in which microbial cells of

Pseudomonas delafieldii were coated with magnetic Fe3O4

nanoparticles (of 10–15 nm) by adsorption was developed by

Shan et al. (2005a). The nanoparticles were strongly adsorbed

onto the cell surfaces because of their high specific surface

area and high surface energy. The magnetic cells were tested

on the biodesulfurization of dibenzothiophene with the

advantage of magnetic separation and reuse.

Biocatalytic properties

To develop a bioprocess, the rates of reactions must be

maximized, thereby substantially reducing capital investment

and operating costs. Applying nanocatalysts is promising due

to their unique properties and large available active surface.

Materials such as gold, which is chemically inert at normal

scales, can serve as a potent chemical catalyst at the

nanoscale. One of the bioprocesses limiting factors is the

mass transfer from an aqueous phase to the surface of the

nanobiocatalyst. Due to their high capacity as sorbents,

nanocatalysts can improve biocatalytic reactions. Adherence

of nanoparticles to cells may enhance the activity of microbes


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(De Windt et al., 2005; Shan et al., 2005b). Some applications

of metal nanoparticles in catalysis were described by Astruc

et al. (2005). Enhancing biodesulfurization through nano-

technology emerges as a revolutionary approach with the

potential of solving some process limitations. Recently, the

application of nanomaterials in biodesulfurization of petrol-

eum products for the production of ultra-low-sulfur products

was described (Shan et al., 2005a,b). Microbial cells of

Pseudomonas delafieldii, coated with magnetic Fe3O4

nanoparticles, showed the same desulfurizing activity as

free cells, but less mass transfer problems (Shan et al., 2005a).

The coated cells had good stability and could be reused

several times. The improvement of the mass transfer rate of

dibenzothiophene (DBT) was shown by Shan et al. (2005b).

Pellet-Rostaing et al. (2005) synthesized highly effective

functional nanomaterials for asymmetric catalysis, deep

desulfurization from gasoline feed and separation of ions.

Xiu et al. (2010) demonstrated that Fe0 nanoparticles could

stimulate methanogenesis, with a �5-fold increase of

methane production (58� 5 to 275� 2 mmol) due to the

increased amount of H2 produced by Fe0. No methane was

detected in the abiotic nanoscale-Fe0 reactor.

Bioavailability and biotransformation of metallicnanoparticles

The interfacial properties of nanoparticles, including the rates

of reactions mediated on the surface, the adsorption capacity

and their redox state affect the geochemical significance of

nanoparticles in the environment (Judy et al., 2011).

Interaction of nanoparticles with naturally occurring colloids,

and particles, could affect their bioavailability and uptake by

organisms. However, little knowledge is available regarding

the bioavailability and biodegradation of nanoparticles, except

for iron. Dissimilatory reduction of ferric iron, a geomicrobial

process occurring in soils, sediments, aquifers and water

bodies, depends on Fe(III) oxyhydroxide minerals as terminal

electron acceptors. The low solubility of Fe(III) oxyhydr-

oxides under near-neutral pH conditions is a challenge for

Fe-related environmental microbiology. A considerable

number of studies are reported on iron NP probably due to

the high abundance of nanosized iron oxides in the environ-

ment, appearing in colloidal suspensions of different aggre-

gate sizes and densities, and to the widespread iron reducing

ability among bacteria.

It is clear that both the intrinsic properties of the particles

(dispersity/stability, shape, crystal structure, size and surface

area) and the environmental conditions (pH, temperature,

presence of organic/inorganic constituents, redox conditions)

determine the behavior of nanoparticles in the environment.

Different particle aggregate sizes might influence the bio-

availability of iron oxides in microbial reduction. Nanosized

aggregates appearing in colloidal suspensions might be

spatially more accessible for microorganisms than large

aggregates flocculating as bulk phases (Bosch et al., 2010).

Microbial reduction of three sizes of hematite nanoparticles

were studied in G. sulfurreducens by Yan et al. (2008) and the

particle aggregation was found to be a major factor for low

reduction rates. The mass normalized reduction rates were

similar for the 10 and 30 nm particles, but lower for the 50 nm

particles. Surface area normalized reduction rates were

highest for 30 nm, indicating that reduction rates are propor-

tional to bacteria-hematite contact area and not to the total

hematite surface area. These results were consistent at two

different partial pressures of H2 (0.01 and 1 atm) and at three

different pH (7, 7.5 and 8). Batch experiments with Geobacter

sulfurreducens and with colloids of ferrihydrite (hydro-

dynamic diameter, 336 nm), hematite (123 nm), goethite

(157 nm) and akaganeite (64 nm) as electron acceptors,

demonstrated that colloidal iron oxides were reduced up to

2 orders of magnitude more rapidly than bulk macroaggre-

gates of the same iron phases (Bosch et al., 2010). Increased

activity was attributed to the large areas of the colloidal

aggregates and higher activity per unit surface, due to the high

bioavailability of the nanosized aggregates.

The effect of size on the bioavailability of hematite

nanoparticles with Pseudomonas mendocina was investigated

by Dehner et al. (2011). Growth of the bacterium was

compared using mass normalized (MN) and surface area

normalized (SAN) nanoparticles, of averages sizes of 8.6 and

72 nm. In both cases, the natural siderophore producing wild

type strain grew faster on 8.6 nm hematite than on 72 nm

hematite. The MN 8.6 nm magnetite has about 6 times larger

surface area per unit mass than the MN 72 nm magnetite

particles, and the higher bioavailability of smaller hematite

particles was attributed to total available surface area and

greater accessibility of the iron to the siderophores.

A siderophore–negative mutant strain was unable to obtain

iron from 72 nm magnetite, while growth was observed with

SAN 8.6 nm magnetite. The authors concluded that, besides a

more rapid siderophore-mediated mechanism, a siderophore-

independent mechanism is capable of supplying Fe from

510 nm hematite to the bacteria. Most probably, the510 nm

particles are capable of penetrating the outer cell wall.

Similarly, wild type and a siderophore-negative mutant of

Pseudomonas aeruginosa PAO1 are able to use ferritin and

ferrihydrate nanoparticles as iron source, suggesting that like

P. mendocina, P. aeruginosa can also acquire iron by

siderophore-independent mechanisms. The secretion of

reductants like pyocyanin have been suggested to mediate

this siderophore-independent iron uptake (Dehner et al.,

2013). Similarly, 6 to 11 times higher methylation rates were

found for surface area normalized HgS nanoparticles as

compared with the microscale particles formed by

Desulfobulbus propionicus 1pr3 and Desulfovibrio desulfur-

icans ND132. Methylation of HgS nanoparticles not only

depends on the surface area but also on their age. The two

sulfate reducers methylated 6–10% of the total mercury aged

for 16 h as compared with only 2–3% of the 3 days or 1 week

older HgS nanoparticles. The reduced availability of aged

nanoparticles may be due to structural changes in aged

nanoparticles (Zhang et al. 2012). During the reduction of

iron(III) oxide by Shewanella algae strain BrY, the initial rate

and reduction extent of various iron(III) oxides (size range

from 2 to 200 nm) was linearly correlated with oxide surface

area (Roden & Zachra, 1996). In marked contrast to other

studies, the surface area normalized Fe(III) reduction rates by

Shewanella onediensis MR-1 for larger (99 nm) particles were

higher when compared with the reduction rates of the smaller

nanoparticles of 11 and 12 nm (Bose et al., 2009).


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Pyrite is considered stable in anoxic geological deposits.

Field observations indicated that anaerobic microbial oxida-

tion of pyrite with nitrate as electron acceptor occurs, but a

direct proof was lacking. Nitrate dependent anaerobic oxida-

tion of pyrite nanoparticles by Thiobacillus denitrificans has

recently been demonstrated (Bosch et al., 2012).

A kinetic model for the reduction of Fe(III) oxyhydroxide

different colloids was developed and validated using

Shewanella putrefaciens 200 R as model organism. The

value of Vmax was found to increase with increasing mineral

solubility (Bonneville et al., 2004). The model predicted that

as the coverage of the outer membrane by nanohematite

increases, the number of reaction centres for electron transfer

from the cell to Fe(III) also increases, which would lead to an

increase of the rate of iron reduction. This prediction was

verified as the initial iron reduction rates were found

proportional to the surface coverage of cells by nanohematite.

More crystallized ferric iron oxides are reduced slower

than the less crystallized forms (Lovley, 1991). In accordance

with this finding, Straub et al. (1998) demonstrate that ferric

iron reducing, Geobacter strains Dfr1 and Dfr 2, and

G. metallireducens were capable of reducing biologically

produced poorly crystallized ferrihydrite into ferrous iron.

Strain Dfr2 was also able to reduce a more crystallized

akaganeite at a slower rate.

The presence of organic matter is another factor influen-

cing the NP behavior and properties in the environment.

For instance, Diogoli et al. (2008) found that organic matter

enhanced Au nanoparticle stability at extreme pH values by

replacing/overcoating the original stabilizer of the nanopar-

ticles. S. putrefaciens utilized the Fe nanoparticles, associated

with organic matter, eight times faster than the nanolepido-

crocite (Pedrot et al., 2011). The increase in bio-reduction was

attributed to humic substances. Indirectly, humic substances

controlled the size, shape and density of oxyhydrooxides and

directly, they mediated as electron shuttle and iron complex-

ation to enhance the Fe bioreduction. These results demon-

strate that, where ever in nature Fe nanoparticles are closely

associated with organic matter, they are much more bioavail-

able and more readily reduced than the crystalline Fe

oxyhydroxides. Recently, adsorptive removal of Ag nanopar-

ticles by Aeromonas punctata have also been demonstrated

(Khan et al. 2012). The rate of adsorption and removal of Ag

nanoparticles was found to decrease with an increase in pH

and salt concentration. Based on this zeta potential study, the

adsorption of the nanoparticles on the bacterial cell surface

was attributed to the electrostatic force of attraction.

Concluding remarks and future perspectives

Nanotechnology is highly interdisciplinary, which requires

collaboration between different sciences and may present

further challenges for environmental scientists and engineers.

In this review, the use of microorganisms in the microbial

synthesis of metallic nanoparticles and the potential applica-

tions in bioremediation were highlighted.

Metallic nanoparticles exhibit unique physical and chem-

ical properties that make them valuable for environmental

biotechnological applications. The growing interest in the use

of superparamagnetic nanoparticles in environmental bio-

remediation may become of great importance in the devel-

opment of new efficient technologies with the possibility to

overcome the weakness of conventional nanoparticles.

Overall, there is still much to do for the improvement of the

nanotechnology systems before its application in bioremedi-

ation and continuous research is needed. The synthesis of

magnetic nanoparticles, covering a wide range of compos-

itions and sizes, has made substantial progress, especially

over the past decade. Nevertheless, an understanding regard-

ing the mechanism of nanoparticle formation is in its infancy.

There is a need to control the size, shape and dispersity, which

would be easier to manipulate if the exact mechanisms of the

formation of nanoparticles are better known. High reprodu-

cibility of biomaterials is also a crucial point to be considered.

Up to now, the formation of mainly Ag, Au, Cd and Pd

nanoparticles has been studied, while knowledge of the

synthesis of other metal nanoparticles is lacking. There is also

a need to explore the microbial diversity to obtain novel

microorganisms on nanoparticles synthesis and to expand the

range of oxide nanoparticles formed by microorganisms.

Currently, neither the exact biochemical mechanism nor the

genes and proteins involved are known. Modern techniques,

like differential proteomics combined with genomics could be

helpful in identifying the key proteins involved in the

nanoparticle synthesis.

For the applicability of nanoparticles during bioremedi-

ation, it is important to develop effective technologies to retain

the nanoparticles in the reactors and to separate and remove

them from the reaction medium after treatment. Future studies

should also aim to extend the number of applications exploring

the maximal characteristics of these new materials.

Thorough cost-benefit analyses are essential to further

evaluate the applicability of nanotechnology. Economic

analyses must take into consideration the synthesis of

nanomaterials, the benefit of application as well as the cost

associated with the potential environmental impacts. Low-

cost nanomaterials should be explored for potential environ-

mental applications. Nanotechnology based water treatment

technologies will only be able to compete with conventional

treatment if the cost of nanomaterials as well as the systems

utilizing nanomaterials becomes comparable.

The studies on bioavailability and biodegradation of

nanoparticles (except iron nanoparticles) are lacking and

need more attention in future. There is dire need for detailed

experiments to determine the extent of nanoparticles bio-

degradability under different environmental conditions (oxic/

anoxic, at different pH and temperatures). Except for one

study, others have shown that nanoparticles are more

bioavailable and degraded faster than the bulk particles.

Bacterial enzymes, like various mono-or dioxygenases

including cytochrome P450 oxygenases, oxidases or peroxid-

ases can oxidize nanomaterials in aerobic environments and

some reductases might be able to reduce them in the

anaerobic environments. Bioavailability is a corner stone in

further assessing risks for ecosystems and human health, and

is therefore an important topic for future nanoparticles

research and their application.


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Declaration of interest

This research was made possible by financial support of the

Chemical Sciences division (CW) of the Netherlands Science

Foundation (NWO) (grant CW-TOP 700.55.343) and the

Spanish Ministry of Education and Science (Consolider-

CSD-00055). AJMS acknowledges the Centre of Biological

Engineering for the invited scientist grant. LJRP holds a

Post-Doc fellowship (SFRH/BPD/20744/2004) from Fundacao

para a Ciencia e Tecnologia.

References

Ahmad, A, Mukherjee, P, Senapatib S, et al. (2003a). Extracellularbiosynthesis of silver nanoparticles using the fungus Fusariumoxysporum. Colloids and Surfaces B: Biointerfaces, 28, 313–8.

Ahmad A, Satyajyoti S, Khan MI, et al. (2003b). Extracellularbiosynthesis of monodisperse gold nanoparticles by a novelextremophilic actinomycete, Thermomonospora sp. Langmuir, 19,3550–3.

Ahmad A, Satyajyoti S, Khan MI, et al. (2003c). Intracellular synthesisof gold nanoparticles by a novel alkalotolerant actinomycete,Rhodococcus species. Nanotechnol, 14, 824–8.

Akbarzadeh A., Samiei M, Davaran S. (2012). Magnetic nanoparticles:preparation, physical properties, and applications in biomedicine.Nanoscale Res Lett, 7, 144–56.

Akin D, Sturgis J, Ragheb K, et al. (2007). Bacteria-mediated delivery ofnanoparticles and cargo into cells. Nature Nanotech, 2, 441–9.

Alphandery E, Carvallo C, Menguy N, Chebbi I. (2011). Chains ofcobalt doped magnetosomes extracted from AMB-1 magnetotacticbacteria for application in alternative magnetic field cancer therapy.J Phys Chem C, 115, 11920–4.

Alvarez LH, Cervantes FJ. (2011). (Bio)nanotechnologies to enhanceenvironmental quality and energy production. J Chem TechnolBiotechnol, 86, 1354–63.

Anceno AJ, Bonduush I, Shipin OV, Dutta J. (2010). Nanoparticle self-assembly via facile (bio)chemistry: charge-stabilized metal nanopar-ticles on microbial cell surfaces. J Bionanosci, 4, 1–6.

Andreu A, Fairweather N, Miller AD. (2008). Clostridium neurotoxinfragments as potential targeting moieties for liposomal gene deliveryto the CNS. Chem Bio Chem, 9, 219–31.

Ansari F, Grigoriev P, Libor S, et al. (2009). DBT degradationenhancement by decorating Rhodococcus erythropolis IGST8 withmagnetic Fe3O4 nanoparticles. Biotech Bioeng, 102, 1505–12.

Astruc D, Lu F, Aranzaes JR. (2005). Nanoparticles as recyclablecatalysts: the fast-growing frontier between homogeneous andheterogeneous catalysts. Angew Chem Int Ed, 44, 7852–72.

Baesman SM, Bullen TD, Dewald J, et al. (2007). Formation of telluriumnanocrystals during anaerobic growth of bacteria that use Teoxyanions as respiratory electron acceptors. Appl EnvironMicrobiol, 73, 2135–43.

Bai HJ, Zhang ZM, Gong J. (2006). Biological synthesis of semicon-ductor zinc sulfide nanoparticles by immobilized Rhodobactersphaeroides. Biotechnol Lett, 28, 1135–9.

Bai HJ, Zhang ZM, Guo Y, Jia W. (2009a). Biological synthesis of size-controlled cadmium sulfide nanoparticles using immobilizedRhodobacter sphaeroides. Nanoscale Res Lett, 4, 717–23.

Bai HJ, Zhang ZM, Guo Y, Yang GE. (2009b). Biosynthesis of cadmiumsulfide nanoparticles by photosynthetic bacteria Rhodopseudomonaspalustris. Coll Surf B, Biointerf, 70, 142–6.

Bai HJ, Zhang ZM. (2009). Microbial synthesis of semiconductor leadsulfide nanoparticles using immobilized Rhodobacter sphaeroides.Mater Lett, 63, 764–6.

Bai HJ, Yang BS, Chai CJ, et al. (2011). Green synthesis of silvernanoparticles using Rhodobacter Sphaeroides. World J MicrobiolBiotechnol, 27, 2723–8.

Bansal V, Rautaray D, Ahmad A, Sastry M. (2004). Biosynthesis ofzirconia nanoparticles using the fungus Fusarium oxysporum. J MaterChem, 14, 3303–5.

Bansal V, Sanyal A, Rautaray D, et al. (2005a). Bioleaching of sand bythe fungus Fusarium oxysporum as a means of producing extracellularsilica nanoparticles. Adv Mater, 17, 889–92.

Bansal V, Rautray D, Bharde A, et al. (2005b). Fungus-mediatedbiosynthesis of silica and titania particles. J Mater Chem, 15, 2583–9.

Bar H, Bhui DK, Sahoo GP, et al. (2009). Green synthesis of silvernanoparticles using latex of Jatropha curcas. Coll Surf A:Physicochem Eng Aspect, 339, 134–9.

Baxter-Plant V, Mikheenko IP, Macaskie LE. (2003). Sulphate-reducingbacteria, palladium and the reductive dehalogenation of chlorinatedaromatic compounds. Biodegradation, 14, 83–90.

Bazylinski DA, Frankel RB, Jannasch HW. (1988). Anaerobic magnetiteproduction by a marine, magnetotactic bacterium. Nature, 334, 518–9.

Bazylinski DA, Garratt-Reed AJ, Abedi A, Frankel RB. (1993). Copperassociation with iron sulfide magnetosomes in a magnetotacticbacterium. Arch Microbiol, 160, 35–42.

Bazylinski DA, Frankel RB. (2004). Magnetosome formation inprokaryotes. Nat Rev Microbiol, 2, 217–30.

Beveridge TJ, Murray RGE. (1980). Sites of metal deposition in the cellwall of Bacillus subtilis. J Bacteriol, 141, 876–87.

Bharde A, Wani A, Shouche Y, et al. (2005). Bacterial aerobic synthesisof nanocrystalline magnetite. J Am Chem Soc, 127, 9326–7.

Bharde A, Rautray D, Bansal V, et al. (2006). Extracellular biosynthesisof magnetite using fungi. Small, 2, 135–41.

Bharde A, Kulkarni A, Rao M, et al. (2007). Bacterial enzyme mediatedbiosynthesis of gold nanoparticles. J Nanosci Nanotechnol, 7,4369–77.

Bhainsa KC, D’Souza SF. (2006). Extracellular biosynthesis of silvernanoparticles using the fungus Aspergillus fumigatus. Coll Surf B:Biointerf, 47, 160–4.

Birla SS, Tiwari VV, Gade AK, et al. (2009). Fabrication of silvernanoparticles by Phoma glomerata and its combined effect againstEscherichia coli, Pseudomonas aeruginosa and Staphylococcusaureus. Lett Appl Microbiol, 27, 76–83.

Blakemore RP. (1975). Magnetotatic bacteria. Science, 190, 377–9.Blakemore RP. (1982). Magnetotatic bacteria. Ann Rev Microbiol, 36,

217–38.Bonneville S, Van Cappellen P, Behrends T. (2004). Microbial reduction

of iron(III) oxyhydroxides, effects of mineral solubility and availabil-ity. Chem Geol, 212, 255–68.

Bosch J, Heister K, Hofmann T, Meckenstock RU. (2010). Nanosizediron oxide colloids strongly enhance microbial iron reduction. ApplEnviron Microbiol, 76, 184–9.

Bosch J, Lee KY, Jordan G, et al. (2012). Anaerobic, nitrate-dependentoxidation of pyrite nanoparticles by Thiobacillus denitrificans.Env Sci Technol, 46, 2095–101.

Bose S, Hochella Jr MF, Gorby YA, et al. (2009). Bioreductionof hematite nanoparticles by the dissimilatory iron reducingbacterium Shewanella oneidensis MR-1. Geochim Cosmochim Acta,73, 962–76.

Bregar VB. (2004). Advantages of ferromagnetic nanoparticle compos-ites in microwave absorbers. IEEE Transact. Magnetics, 40, 1679–84.

Bucak S, Jones DA, Laibinis PE, Hatton TA. (2003). Protein separationsusing colloidal magnetic nanoparticles. Biotechnol Prog, 19, 477–84.

Bunge M, Sobjerg LS, Rotaru AE, et al. (2010). Formation ofpalladium(0) nanoparticles at microbial surfaces. Biotechnol Bioeng,107, 206–15.

Cameron CT, Reese RN, Mehra RK, et al. (1989). Biosynthesis ofcadmium sulfide quantum semiconductor crystallites. Nature, 338,596–7.

Chan CS, De Stasio G, Weich SA, et al. (2004). Microbial polysac-charides template assembly of nanocrystal fibers. Science, 303,1656–8.

Chang YC, Chen DH. (2005a). Preparation and adsorption properties ofmonodisperse chitosan-bound Fe3O4 magnetic nanoparticles forremoval of Cu(II) ions. J Coll Interf Sci, 283, 446–51.

Chang YC, Chen DH. (2005b). Adsorption kinetics and thermodynamicsof acid dyes on a carboxymethylated chitosan-conjugated magneticnano-adsorbent. Macromol Bioscience, 5, 254–61.

Che G, Lakshmi BB, Fisher ER, Martin CR. (1998). Carbon nanotubulemembranes for electrochemical energy storage and production.Nature, 393, 346–8.


Cri

tical

Rev

iew

s in

Bio

tech

nolo

gy D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y 21

3.22

.239

.223

on

08/2

3/13

For

pers

onal

use

onl

y.

Chen Z, Gao L. (2007). A facile and novel way for the synthesis of nearlymonodisperse silver nanoparticles. Mater Res Bulletin, 42, 1657–61.

Chidambaram D, Hennebel T, Taghavi S, et al. (2010). Concomitantmicrobial generation of palladium nanoparticles and hydrogen toimmobilize chromate. Environ Sci Technol, 44, 7635–40.

Chirita M, Grozescu I. (2009). Fe2O3 – Nanoparticles, physicalproperties and their photochemical and photoelectrochemical appli-cations. Chem Bull, 54, 1–8.

Coker VS, Telling ND, van der Laan G, et al. (2013). Harnessing theextracellular bacterial production of nanoscale cobalt ferrite withexploitable magnetic properties. ACS Nano, 3, 1922–8.

Creamer NJ, Mikheenko IP, Yong P, et al. (2007). Novel supported Pdhydrogenation bionanocatalyst for hybrid homogeneous/heteroge-neous catalysis. Catal Today, 128, 80–7.

Cunningham DP, Lundie LL. (1993). Precipitation of cadmium byClostridium thernoaceticum. Appl Environ Microbiol, 59, 7–14.

De Windt W, Aelterman P, Verstraete W. (2005). Bioreductive depos-ition of palladium (0) nanoparticles on Shewanella oneidensis withcatalytic activity towards reductive dechlorination of polychlorinatedbiphenyls. Environ Microb, 7, 314–25.

Deepak V, Umamaheshwaran PS, Guhan K, et al. (2011). Synthesis ofgold and silver nanoparticles using purified URAK. Coll Surf B,Biointerf, 86, 353–8.

Dehner CA, Barton L, Maurice PA, Dubois JL. (2011). Size-dependentbioavailability of hematite (a-Fe2O3) nanoparticles to a commonaerobic bacterium. Environ Sci Technol, 45, 977–83.

Dehner C, Morales-Soto N, Behera RK, et al. (2013). Ferritin andferrihydrite nanoparticles as iron sources for Pseudomonas aerugi-nosa. J Biol Inorg Chem, 18, 371–81.

Deplanche K, Macaskie LE. (2008). Biorecovery of gold by Escherichiacoli and Desulfovibrio desulfuricans. Biotechnol Bioeng, 99,1055–64.

Deplanche K, Caldelari I, Mikheenko IP, et al. (2010). Involvement ofhydrogenases in the formation of highly catalytic Pd(0) nanoparticlesby bioreduction of Pd(II) using Escherichia coli mutant strains.Microbiology, 156, 2630–40.

Derjaguin B, Landau L. (1945). Theory of highly charged lyophobic solsand adhesion of highly charged-particles in solutions of electrolytes.Hurnal Eksperimentallnoi I Teoreticheskoi Fiziki, 15, 663–82.

Derjaguin B, Landau L. (1993). Theory of the stability of stronglycharged lyophobic sols and of the adhesion of strongly charged-particles in solutions of electrolytes. Progress Surf Sci, 43, 30–59.

Diegoli S, Manciulea AL, Begum S, et al. (2008). Interaction betweenmanufactured gold nanoparticles and naturally occurring organicmacromolecule. Sci Tot Environ, 402, 51–61.

Duran N, Marcato PD, Alves OL, et al. (2005). Mechanistic aspects ofbiosynthesis of silver nanoparticles by several Fusarium oxysporumstrains. J Nanobio-technol, 3, 1–7.

Eltzholtz JR, Iversen BB. (2011). High-temperature and high-pressurepulsed synthesis apparatus for supercritical production of nanoparti-cles. Rev Sci Instrum, 82, 84–102.

Evanoff DD, Chumanov G. (2004). Size-controlled synthesis ofnanoparticles. 1. ‘‘Silver-only’’ aqueous suspensions via hydrogenreduction. J Phys Chem B, 108, 13948–56.

Ewert KK, Evans HM, Bouxsein NF, Safinya CR. (2006). Dendriticcationic lipids with highly charged headgroups for efficient genedelivery. Bioconjugate Chem, 17, 877–88.

Fan Y, Xu S, Schaller R, et al. (2010). Nanoparticle decorated anodes forenhanced current generation in microbial electrochemical cells.Biosens Bioelectron, 26, 1908–12.

Faraji M, Yamini Y, Tahmasebi E, et al. (2010).Cetyltrimethylammonium bromide-coated magnetite nanoparticlesas highly efficient adsorbent for rapid removal of reactive dyesfrom the textile companies’ wastewaters. J Iran Chem Soc, 7,S130–44.

Faria PCC, Orfao JJM, Pereira MFR. (2005). Mineralisation of colouredaqueous solutions by ozonation in the presence of activated carbon.Water Res, 39, 1461–70.

Faria PCC, Orfao JJM, Figueiredo JL, Pereira MFR. (2008). Adsorptionof aromatic compounds from the biodegradation of azo dyes onactivated carbon. Appl Surf Sci, 254, 3497–503.

Farre M, Gajda-Schrantz K, Kantiani L, Barcelo D. (2009). Ecotoxicityand analysis of nanomaterials in the aquatic environment. AnalBioanal Chem, 393, 81–95.

Feng Y, Yu Y, Wang Y, Lin X. (2007). Biosorption and Bioreduction ofTrivalent Aurum by Photosynthetic Bacteria Rhodobacter capsulatus.Curr Microbiol, 55, 402–8.

Fu M, Li Q, Sun D, et al. (2006). Rapid preparation process of silvernanoparticles by bioreduction and their characterizations. Chinese JChem Eng, 14, 114–7.

Gade AK, Bonde P, Ingle AP, et al. (2008). Exploitation of Aspergillusniger for synthesis of silver nanoparticles. J Biobased Mater Bioen, 2,243–7.

Gauthier D, Sobjerg LS, Jensen KM, et al. (2010). Environmentallybenign recovery and reactivation of palladium from industrial wasteby using gram-negative bacteria. Chem Sus Chem, 3, 1036–9.

Gurunathan S, Kalishwaralal K, Vaidyanathan R, et al. (2009).Biosynthesis, purification and characterization of silver nanoparticlesusing Escherichia coli. Coll Surf B, Biointerf, 74, 328–35.

Harada M, Abe D, Kimura Y. (2005). Synthesis of colloidal dispersionsof rhodium nanoparticles under high temperatures and high pressures.J Colloid Interface Sci, 292, 113–21.

Hashemian S. (2010). MnFe2O4/bentonite nano composite as a novelmagnetic material for adsorption of acid red 138. African JBiotechnol, 9, 8667–71.

Hashimoto H, Yokoyama S, Asaoka H, et al. (2007). Characteristics ofhollow microtubes consisting of amorphous iron oxide nanoparticlesproduced by iron oxidizing bacteria, Leptothrix ochracea. J MagnMagn Mater, 310, 2405–7.

He F, Zhao A. (2005). Preparation and characterization of a new class ofstarch-stabilized bimetallic nanoparticles for degradation of chlori-nated hydrocarbons in water. Environ Sci Technol, 39, 3314–20.

He F, Zhao A. (2007). Manipulating the size and dispersibility ofzerovalent iron nanoparticles by use of carboxymethyl cellulosestabilizers. Environ Sci Technol, 41, 6216–21.

He SY, Guo ZR, Zhang Y, et al. (2007). Biosynthesis of goldnanoparticles using the bacteria Rhodopseudomonas capsulata.Mater Lett, 61, 3984–7.

He S, Zhang Y, Guo Z, Gu N. (2008). Biological synthesis of goldnanowires using extract of Rhodopseudomonas capsulata. BiotechnolProg, 24, 476–80.

Hennebel T, Simoen H, De Windt W, et al. (2009). Biocatalyticdechlorination of trichloroethylene with bio-palladium in a pilot-scalemembrane reactor. Biotechnol Bioengin, 102, 995–1002.

Hennebel T, Van Nevel S, Verschuere S, et al. (2011). Palladiumnanoparticles produced by fermentatively cultivated bacteria ascatalyst for diatrizoate removal with biogenic hydrogen. ApplMicrobiol Biotechnol, 91, 1435–45.

Holmes JD, Richardson DJ, Saed S, et al. (1997). Cadmium-specificformation of metal sulfide ‘Q-particles’ by Klebsiella pneumoniae.Microbiol, 143, 2521–30.

Hristovski K, Baumgardener A, Westerhoff P. (2007). Selecting metaloxide nanomaterials for arsenic removal in fixed bed columns: fromnanopowders to aggregated nanoparticle media. J Hazard Mater, 147,265–74.

Huang CP, Juang CP, Morehart K, Allen L. (1990). The removal of Cu(II) from dilute aqueous solutions by Saccharomyces cerevisiae.Wat Res, 24, 433–9.

Humphries AC, Macaskie LE. (2005). Reduction of Cr(VI) by palladizedbiomass of Desulfovibrio vulgaris NCIMB 8303. J Chem TechnolBiotechnol, 80, 1378–82.

Ingle A, Rai MK, Gade A, Bawaskar M. (2009). Fusarium solani: anovel biological agent for the extracellular synthesis of silvernanoparticles. J Nanop Res, 11, 2079–85.

Jain PK, Huang X, El-Sayed IH, El-Sayed MA. (2008). Noble metals onthe nanoscale: optical and photothermal properties and some appli-cations in imaging, sensing, biology, and medicine. Acc Chem Res,41, 1578–86.

Jain D, Kachhwaha S, Jain R, et al. (2010). Novel microbial route tosynthesize silver nanoparticles using spore crystal mixture of Bacillusthuringiensis. India J Exp Biol, 48, 1152–6.

Jha AK, Prasad K, Kulkarni AR. (2009). Synthesis of TiO2 nanoparticlesusing microorganisms. Coll Surf B, 71, 226–9.

Jogler C, Schuler D. (2009). Genomics, genetics, and cell biology ofmagnetosome formation. Annu Rev Microbiol, 63, 501–21.

Jucker BA, Zehnder AJB, Harms H. (1998). Quantification ofpolymer interactions in bacterial adhesion. Env Sci Technol, 32,2909–15.


Cri

tical

Rev

iew

s in

Bio

tech

nolo

gy D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y 21

3.22

.239

.223

on

08/2

3/13

For

pers

onal

use

onl

y.

Judy JD, Unrine JM, Bertsch PM. (2011). Evidence for biomagnificationof gold nanoparticles within a terrestrial food chain. Environ SciTechnol, 45, 776–81.

Juibari MM, Abbasalizadeh S, Jouzani GS, Noruzi M. (2011). Intensifiedbiosynthesis of silver nanoparticles using a native extremophilicUreibacillus thermosphaericus strain. Mat Lett, 65, 1014–7.

Kalimuthu K, Babu RS, Venkataraman D, et al. (2008). Biosynthesis ofsilver nanocrystals by Bacillus licheniformis. Coll Surf B Biointerf,65, 150–3.

Kannan N, Mukunthan KS, Balaji S. (2011). A comparative study ofmorphology, reactivity and stability of synthesized silver nanoparti-cles using Bacillus subtilis and Catharanthus roseus (L.) G. Don.CollSurf B Biointerf, 86, 378–83.

Kashefi K, Tor JM, Nevin KP, Lovley DR. (2001). Reductive precipi-tation of gold by dissimilatory Fe(III)-reducing bacteria and archaea.Appl Environ Microbiol, 67, 3275–9.

Khaleel A, Kapoor PN, Klabunde KJ. (1999). Nanocrystalline metaloxides as new adsorbents for air purification. Nanostruct Mater, 11,459–68.

Khan SS, Mukherjee A, Chandrasekaran N. (2012). Adsorptive removalof silver nanoparticles (SNPs) from aqueous solution by Aeromonaspunctata and its adsorption isotherm and kinetics. Colloids Surf BBiointerfaces, 92, 156–60.

Kim J, Grate JW. (2005). Nano-biotechnology in using enzymes forenvironmental remediation: single-enzyme nanoparticles. In: Karn B,Masciangioli T, Zhang W, Colvin V, Alivisatos P, eds. ACSSymposium Series: Nanotechnology and the environment: applica-tions and implications, Washington, D.C., 220–5.

Klaus T, Joerger R, Olsson E, Granqvist CG. (1999). Silver-basedcrystalline nanoparticles, microbially fabricated. Proc Natl Acad SciUSA, 96, 13611–4.

Ko CH, Park JG, Park JC, et al. (2007). Surface status and sizeinfluences of nickel nanoparticles on sulfur compound adsorption.Appl Surf Sci, 253, 5864–7.

Koebel MM, Jones LC, Somorjai GA. (2008). Preparation of size-tunable, highly monodisperse PVP-protected Pt-nanoparticles by seed-mediated growth. J Nanop Res, 10, 1063–9.

Koneracka M, Kopcansky P, Timko M et al. (2006). Immobilization ofenzymes on magnetic particles. In: Guisan JM, ed. Methods inbiotechnology: immobilization of enzymes and cells. Totowa:Hummana Press Inc, 217–228.

Konishi Y, Ohno K, Saitoh N, et al. (2007a). Bioreductive depositionof platinum nanoparticles on the bacterium Shewanella algae.J Biotechnol, 128, 648–53.

Konishi Y, Tsukiyama T, Tachimi T, et al. (2007b). Microbial depositionof gold nanoparticles by the metal-reducing bacterium Shewanellaalgae. Electrochim Acta, 53, 186–92.

Kowshik N, Vogel W, Kulkarni SK, et al. (2002). Microbial synthesisof semiconductors CdS nanoparticles, their characterizationand their use in the fabrication of ideal diode. Biotechnol Bioeng,87, 583.

Krumov N, Odera S, Perner-Nochta I, et al. (2007). Accumulation ofCdS nanoparticles by yeasts in a fed-batch bioprocess. J Biotechnol,132, 481–6.

Krumov N, Perner-Nochta I, Oder S, et al. (2009). Production ofinorganic nanoparticles by microorganisms. Chem Eng Technol, 32,1026–35.

Kubo T, Sugita T, Shimose S, et al. (2000). Targeted deliveryof anticancer drugs with intravenously administered magneticliposomes in osteosarcoma-bearing hamsters. Int J Oncol, 17,309–16.

Kumar SA, Abyaneh MK, Gosavi SW, et al. (2007a). Nitrate reductase-mediated synthesis of silver nanoparticles from AgNO3. BiotechnolLett, 29, 439–45.

Kumar SA, Abyaneh MK, Gosavi SW, et al. (2007b). Sulfite reductase-mediated synthesis of gold nanoparticles capped with phytochelatin.Biotechnol Appl Biochem, 47, 191–5.

Kumar U, Shete A, Harle AS, et al. (2008). Extracellular bacterialsynthesis of protein-functionalized ferromagnetic Co3O4 nanocrystalsand imaging of self-organization of bacterial cells under stress afterexposure to metal ions. Chem Mater, 20, 1484–91.

Kumar CG, Mamidyala SK, Das B, et al. (2010). Synthesis ofbiosurfactant-based silver nanoparticles with purified rhamnolipidsisolated from Pseudomonas aeruginosa BS-161R. J MicrobiolBiotechnol, 20, 1061–8.

Kumar CG, Mamidyala SK. (2011). Extracellular synthesis of silvernanoparticles using culture supernatant of Pseudomonas aeruginosa.Coll Surf B Biointerf, 84, 462–6.

Lee JH, Huh YM, Jun YW, et al. (2006). Artificially engineeredmagnetic nanoparticles for ultra-sensitive molecular imaging. NatureMed, 13, 95–9.

Lee D, Khaja S, Velasquez-Castano JC, et al. (2007). In vivo imaging ofhydrogen peroxide with chemiluminescent nanoparticles. NatureMater, 6, 765–9.

Lee C, Kim JY, Lee WI, et al. (2008). Bactericidal effect of zero-valentiron nanoparticles on Escherichia coli. Environ Sci Technol, 42,4927–33.

Lee C, Sedlak DL. (2008). Enhanced formation of oxidants frombimetallic nickel-iron nanoparticles in the presence of oxygen.Environ Sci Technol, 42, 8528–33.

Lengke M, Fleet ME, Southam G. (2006a). Morphology ofgold nanoparticles synthesized by filamentous cyanobacteria fromgold(I)-thiosulfate and gold(III)-chloride complexes. Langmuir, 22,2780–7.

Lengke M, Ravel B, Fleet ME, et al. (2006b). Mechanisms of goldbioaccumulation by filamentous cyanobacteria from gold(III)-chloridecomplex. Environ Sci Technol, 40, 6304–9.

Lengke M, Southam G. (2006). Bioaccumulation of gold by sulfate-reducing bacteria cultured in the presence of gold(I)-thiosulfatecomplex. Geochim Cosmochim Acta, 70, 3646–61.

Lengke MF, Fleet ME, Southam G. (2007). Synthesis of palladiumnanoparticles by reaction of filamentous cyanobacterial biomass witha palladium(II) chloride complex. Langmuir, 23, 8982–7.

Li B, Du Y, Dong S. (2009). DNA based gold nanoparticles colorimetricsensors for sensitive and selective detection of Ag(I) ions. Anal ChimActa, 644, 78–82.

Ling L, Maohong F, Robert B, et al. (2006). Synthesis, Properties andenvironmental applications of nanoscale iron-based materials: areview. Crit Rev Environ Sci Technol, 36, 405–31.

Liu X, Xing J, Guan Y, et al. (2004). Synthesis of amino-silane modifiedsuperpara-magnetic silica supports and their use for protein immo-bilization. J Coll Surf A, 238, 127–31.

Liu WT. (2006). Nanoparticles and their biological and environmentalapplications. J Biosci Bioeng, 102, 1–7.

Liskowitz JJ, Liskowitz MJ, Chen S. (2009). Reactive atomized zerovalent iron enriched with sulfur and carbon to enhance corrosivity andreactivity of the iron and provide desirable reduction products. Patentapplication number: 20090191084. http://www.faqs.org/patents/app/20090191084.

Lloyd JR, Yong P, Macaskie LE. (1999). Enzymatic recovery ofelemental palladium by using sulfate-reducing bacteria. Appl EnvironMicrobiol, 64, 4607–9.

Lovley DR, Stolz JF, Nord GL, Phillips EJP. (1987). Anaerobicproduction of magnetite by a dissimilatory iron reducing microorgan-ism. Nature, 330, 252–4.

Lovley DR. (1991). Dissimilatory Fe(III) and Mn(IV) reduction.Microbiol Ver, 55, 259–87.

Luef B, Fakra SC, Csencsits R, et al. (2013). Iron-reducing bacteriaaccumulate ferric oxyhydroxide nanoparticle aggregates that maysupport planktonic growth. ISME J, 7, 338–50.

Lukhele LP, Bhekie BM, Momba MNB, Krause RWM. (2010). Waterdisinfection using novel cyclodextrin polyurethanes containing sil-ver nanoparticles supported on carbon nanotubes. J Appl Sci, 10,65–70.

Ma H, Yin B, Wang S, et al. (2004). Synthesis of silver and goldnanoparticles by a novel electrochemical method. Chem Phys Chem,5, 68–75.

Mak SY, Chen DH. (2004). Fast adsorption of methylene blue onpolyacrylic acid-bound iron oxide magnetic nanoparticles. Dyes Pig,61, 93–8.

Malik PK. (2004). Dye removal from wastewater using activated carbondeveloped from sawdust: adsorption equilibrium and kinetics.J Hazard Mater B, 113, 81–8.

Mandal S, Selvakannan PR, Phadtare S, et al. (2002). Synthesis of astable gold hydrosol by the reduction of chloroaurate ions by theamino acid, aspartic acid. Proc Indian Acad Sci (Chem Sci), 114,513–20.

Mann S, Sparks NHC, Frankel RB, et al. (1990). Biomineralization offerromagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magneto-tactic bacterium. Nature, 343, 258–61.


Cri

tical

Rev

iew

s in

Bio

tech

nolo

gy D

ownl

oade

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lthca

re.c

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http://www.faqs.org/patents/app/20090191084

http://www.faqs.org/patents/app/20090191084

Marre S, Baek J, Park J, et al. (2009). High-pressure/high-temperaturemicroreactors for nanostructure synthesis. J Labor Autom, 14, 367–74.

Marshall MJ, Beliaev AS, Dohnalkova AC, et al. (2006). c-Typecytochrome-dependent formation of U(IV) nanoparticles byShewanella oneidensis. PLoS Biol, 4, 1324–33.

Marshall MJ, Plymale AE, Kennedy DW, et al. (2008). Hydrogenase-and outer membrane c-type cytochrome-facilitated reduction oftechnetium(VII) by Shewanella oneidensis MR-1. EnvironMicrobiol, 10, 125–36.

Masciangioli T, Zhang WX. (2003). Environmental technologies at thenanoscale. Environm Sci Technol, 37, 102A–8A.

Mikheenko IP, Rousset M, Dementin S, Macaskie LE. (2008).Bioaccumulation of palladium by Desulfovibrio fructosivorans wild-type and hydrogenase-deficient strains. Appl Environ Microbiol, 74,6144–6.

Mokhtari N, Daneshpajouh S, Seyedbagheri S, et al. (2009). Biologicalsynthesis of very small silver nanoparticles by culture supernatant ofKlebsiella pneumonia, the effects of visible-light irradiation and theliquid mixing process. Mater Res Bull, 44, 1415–21.

Moon J-W, Yeary LW, Rondinone AJ, et al. (2007). Magnetic responseof microbially synthesized transition metal- and lanthanide-substitutednanosized magnetites. J Magn Magn Mater, 313, 283–92.

Moores A, Goettmann F. (2006). The plasmon band in noble metalnanoparticles: an introduction to theory and applications. New JChem, 30, 1121–32.

Mosiniewicz-Szablewska E, Safarikova M, Safarik I. (2009). Magneticstudies of ferrofluid-modified microbial cells. J Nanosci Nanotechnol,10, 2531–36.

Moskowitz BM, Bazylinski DA, Egli R, et al. (2008). Magnetic propertiesof marine magnetotactic bacteria in a seasonally stratified coastal pond(Salt Pond, MA, USA). Geophys J Int, 174, 75–92.

Mukherjee P, Ahmad A, Mandal D, et al. (2001). Bioreduction of AuCl�4ions by the fungus Verticillium sp and surface trapping of the goldnanoparticles formed. Angew Chem Int Ed, 40, 3585–8.

Mukherjee P, Senapati S, Mandal D, et al. (2002). ExtracellularSynthesis of Gold Nanoparticles by the Fungus Fusarium oxysporum.Chem Bio Chem, 3, 461–3.

Murawala P, Phadnis SM, Bhonde RR, Prasad BLV. (2009). In situsynthesis of water dispersible bovine serum albumin capped gold andsilver nanoparticles and their cytocompatibility studies. Coll Surf BBiointerf, 73, 224–8.

Nair B, Pradeep T. (2002). Coalescence of nanoclusters and formation ofsubmicron crystallites assisted by Lactobacillus strains. Cryst GrowthDes, 2, 293–8.

Namasivayam SKR, Gnanendra KE, Reepika R. (2010). Synthesis ofsilver nanoparticles by Lactobacillus acidophilus 01 strain andevaluation of its in vitro genomic DNA toxicity. Nano-Micro Lett, 2,160–3.

Nangia Y, Wangoo N, Sharma S, et al. (2009). Facile biosynthesis ofphosphate capped gold nanoparticles by a bacterial isolateStenotrophomonas maltophilia. Appl Phys Lett, 94, 233901.

Neal AL. (2008). What can be inferred from bacterium–nanoparticleinteractions about the potential consequences of environmentalexposure to nanoparticles? Ecotoxicol, 17, 362–71.

Ng CK, Sivakumar K, Liu X et al. (2013). Influence of outer membranec-type cytochromes on particle size and activity of extracellularnanoparticles produced by Shewanella oneidensis. Biotechnol Bioeng,DOI 10.1002/bit.24856.

Noubactep C. (2010). The fundamental mechanism of aqueous contam-inant removal by metallic iron. Water SA, 36, 663–70.

Ogi T, Saitoh N, Nomura T, Konishi Y. (2010). Room-temperaturesynthesis of gold nanoparticles and nanoplates using Shewanellaalgae cell extract. J Nanopart Res, 12, 2531–9.

Oliveira LCA, Rios RVRA, Fabris JD, et al. (2002). Activated carbon/iron oxide magnetic composites for the adsorption of contaminants inwater. Carbon, 40, 2177–83.

Overbeek T. (1999). DLVO theory – Milestone of 20th century colloidscience – Preface. Adv Coll Interf Sci, 83, IX–XI.

Parikh RY, Singh S, Prasad BLV, et al. (2008). Extracellular synthesis ofcrystalline silver nanoparticles and molecular evidence of silverresistance from Morganella sp., towards understanding biochemicalsynthesis mechanism. Chem Bio Chem, 9, 1415–22.

Patnaik S, Arif M, Pathak A, et al. (2010). Cross-linked polyethyleni-mine-hexametaphosphate nanoparticles to deliver nucleic acidstherapeutics. Nanomedicine: Nanotechnol Biol Med, 6, 344–54.

Pedrot M, Le Boudec A, Davranche M, et al. (2011). How does organicmatter constrain the nature, size and availability of Fe nanoparticlesfor biological reduction?. J Colloid Interface Sci, 359, 75–85.

Pellet-Rostaing S, Favre-Reguillon A, Lemaire M. (2005). Smartnanomaterials for asymmetric catalysis, deep desulfurization ofgas oils and ion separation. Actualite Chimique, 98–107. (Suppl):290–291.

Ponder SM, Darab JG, Bucher J, et al. (2001). Surface chemistry andelectrochemistry of supported zerovalent iron nanoparticles inthe remediation of aqueous metal contaminants. Chem Mater, 13,479–86.

Posfai M, Buseck PR, Bazylinski DA, Frankel RB. (1998). Iron sulfidesfrom magnetotactic bacteria, structure, composition, and phasetransitions. Am Mineral, 83, 1469–81.

Prakash A, Sharma S, Ahmad N, et al. (2010). Bacteria mediatedextracellular synthesis of metallic nanoparticles. Int Res J Biotechnol,1, 71–9.

Prasad K, Jha AK, Kulkarni AR. (2007). Lactobacillus assisted synthesisof titanium nanoparticles. Nanoscale Res Lett, 2, 248–50.

Prasad K, Jha AK, Prasad K, Kulkarni AR. (2010). Can microbesmediate nano-transformation?. Indian J Phys, 84, 1355–60.

Qu S, Huang F, Yu S, et al. (2008). Magnetic removal of dyes fromaqueous solution using multi-walled carbon nanotubes filled withFe2O3 particles. J Hazard Mater, 160, 643–7.

Rai M, Durn N. (2011). Metal Nanoparticles in Microbiology. London,Springer.

Ramanathan R, Field MR, O’Mullane AP, et al. (2013). Aqueous phasesynthesis of copper nanoparticles: a link between heavy metalresistance and nanoparticle synthesis ability in bacterial systems.Nanoscale, 5, 2300–6.

Rangnekar A, Sarma TK, Singh AK, et al. (2007). Retention ofenzymatic activity of a-amylase in the reductive synthesis of goldnanoparticles. Langmuir, 23, 5700–6.

Ranzoni A, Sabatte G, van Ijzendoorn LJ, Prins MW. (2012). One-stephomogeneous magnetic nanoparticle immunoassay for biomarkerdetection directly in blood plasma. ACS Nano, 6, 3134–41.

Rautaray D, Ahmad A, Sastry M. (2004). Biological synthesis of metalcarbonate minerals using fungi and actinomycetes. J Mater Chem, 14,2333– 40.

Rawat M, Singh D, Saraf S., Saraf S. (2006). Nanocarriers: promisingvehicle for bioactive drugs. Biol Pharm Bull, 29, 1790–8.

Reddy KR. (2010). Nanotechnology for site remediation: dehalogenationof organic pollutants in soils and groundwater by nanoscale ironparticles. 6th International Congress on Environmental Geotechnics,2010, New Delhi, India, pp 165–82.

Redwood MD, Deplanche K, Baxter-Plant VS, Macaskie LE. (2008).Biomass-supported palladium catalysts on Desulfovibrio desulfuri-cans and Rhodobacter sphaeroides. Biotechnol Bioeng, 99, 1045–54.

Riddin TL, Gericke M, Whiteley CG. (2006). Analysis of the inter- andextracellular formation of platinum nanoparticles by Fusariumoxysporum f sp lycopersici using response surface methodology.Nanotechnol, 17, 3482–9.

Rijnaarts HHM, Norde W, Lyklema J, Zehnder AJB. (1995a). Theisoelectric point of bacteria as an indicator for the presence of cellsurface polymers that inhibit adhesion. Coll Surf B: Biointerf, 4,191–7.

Rijnaarts HHM, Norde W, Bouwer EJ, et al. (1995b). Reversibility andmechanism of bacterial adhesion. Coll Surf B: Biointerf, 4, 5–22.

Rijnaarts HHM, Norde W, Lyklema J, Zehnder AJB. (1999). DLVO andsteric contributions to bacterial deposition in media of different ionicstrengths. Coll Surf B: Biointerf, 14, 179–95.

Roden EE, Zachara JM. (1996). Microbial reduction of crystallineiron(III) oxides, influence of oxide surface area and potential for cellgrowth. Environ Sci Technol, 30, 1618–28.

Roh Y, Lauf RJ, McMillan AD, et al. (2001). Microbial synthesis and thecharacterization of metal substituted magnetites. Solid State Commun,118, 529–34.

Ryu J, Kim SW, Kang K, Park CB. (2010). Synthesis of diphenylalanine/cobalt oxide hybrid nanowires and their application to energy storage.ACS Nano, 4, 159–64.

Safarik I, Safarikova M. (2007). Magnetically modified microbial cells: Anew type of magnetic adsorbents. China Particuology, 5, 19–25.

Safarikova M, Ptackova L, Kibrikova I, Safarik I. (2005). Biosorption ofwater-soluble dyes on magnetically modified Saccharomyces cerevi-siae subsp. uvarum cells. Chemosphere, 59, 831–5.


Cri

tical

Rev

iew

s in

Bio

tech

nolo

gy D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y 21

3.22

.239

.223

on

08/2

3/13

For

pers

onal

use

onl

y.

Safarikova M, Pona BMR, Mosinicwicz Szablewska E, et al. (2008).Dye adsorption on magnetically modified Chlorella vulgaris cells.Fres Environ Bulletin, 17, 486–92.

Safarikova M, Maderova Z, Safarik I. (2009). Ferrofluid modifiedSaccharomyces cerevisiae cells for biocatalysis. Food Res Int, 42,521–4.

Saifuddin N, Wong CW, Yasumira AAN. (2009). Rapid biosynthesis ofsilver nanoparticles using culture supernatant of bacteria withmicrowave irradiation. Eur J Chem, 6, 61–70.

Sakaguchi T, Burgess JG, Matsunaga T. (1993). Magnetite formation bya sulphate reducing bacterium. Nature, 365, 47–9.

Selvakannan PR, Swami A, Srisathiyanarayanan D, et al. (2004).Synthesis of aqueous Au core�Ag shell nanoparticles using tyrosineas a pH-dependent reducing agent and assembling phase-transferredsilver nanoparticles at the air�water interface. Langmuir, 20, 7825–36.

Shahverdi AR, Minaeian S, Shahverdi HR, et al. (2007). Rapid synthesisof silver nanoparticles using culture supernatants of Enterobacteria, anovel biological approach. Proc Biochem, 42, 919–23.

Shan GB, Xing JM, Luo MF, et al. (2003). Immobilization ofPseudomonas delafieldii R-8 with magnetic polyvinyl alcohol beadsand its application in biodesulfurization. Biotechnol Lett, 25,1977–81.

Shan GB, Xing JM, Zhang HY, Liu HZ. (2005a). Biodesulfurization ofdibenzothiophene by microbial cells coated with magnetite nanopar-ticles. Appl Environ Microbiol, 71, 4497–502.

Shan GB, Zhang HY, Cai W, et al. (2005b). Improvement ofbiodesulfurization rate by assembling nanosorbents on the surfacesof microbial cells. Biophysical J, 89, 58–60.

Sharma YC, Srivastava V, Upadhyay SN, Weng CH. (2008). Aluminananoparticles for the removal of Ni(II) from aqueous solutions. IndEng Chem Res, 47, 8095–100.

Sharma YC, Srivastava V, Weng CH, Upadhyay SN. (2009). Removal ofCr(VI) From Wastewater by Adsorption on Iron Nanoparticles.Canadian J Chem Eng, 87, 921–9.

Shin KH, Cha DK. (2008). Microbial reduction of nitrate in the presenceof nanoscale zero-valent iron. Chemosphere, 72, 257–62.

Sinha A, Khare SK. (2011). Mercury bioaccumulation and simultaneousnanoparticle synthesis by Enterobacter sp. cells. Bioresour Technol,102, 4281–4.

Sintubin L, De Windt W, Dick J, et al. (2009). Lactic acid bacteria asreducing and capping agent for the fast and efficient production ofsilver nanoparticles. Appl Microbiol Biotechnol, 84, 741–9.

Staniland S, Williams W, Telling N, et al. (2008). Controlled cobaltdoping of magnetosomes in vivo. Nat Nanotechnol, 3, 158–62.

Straub KL, Hanzlik M, Buchholz-Cleven BEE. (1998). The use ofbiologically produced ferrihydrate for the isolation of novel iron-reducing bacteria. System Appl Microbiol, 21, 442–9.

Sun YP, Li X, Cao J, et al. (2006). Characterization of zero-valent ironnanoparticles. Adv Coll Interf Sci, 120, 47–56.

Sun S, Ma M, Qiu N, et al. (2011). Affinity adsorption and separationbehaviors of avidin on biofunctional magnetic nanoparticles bindingto iminobiotin. Coll Surf B: Biointerf, 88, 246–53.

Suzuki Y, Kelly SD, Kemner KM, Banfield JF. (2002). Nanometre-sizeproducts of uranium bioreduction. Nature, 419, 134.

Sweeney RY, Mao C, Gao X, et al. (2004). Bacterial biosynthesis ofcadmium sulfide nanocrystals. Chem Biol, 11, 1553–9.

Tanaka M, Arakaki A, Staniland SS, Matsunaga T. (2010).Simultaneously discrete biomineralization of magnetite and telluriumnanocrystals in magnetotactic bacteria. Appl Environ Microbiol,7616, 5526–32.

Tao AR, Habas S, Yang P. (2008). Shape control of colloidal metalnanocrystals. Small, 4, 310–25.

Towe KM, Moench TT. (1981). Electron-optical characterization ofbacterial magnetite. Earth Planet Sci Lett, 52, 213–20.

Tsang SC, Yu CH, Gao X, Tam K. (2006). Silica-encapsulatednanomagnetic particle as a new recoverable biocatalyst carrier.J Phys Chem B, 110, 16914–22.

Tungittiplakornw W, Cohenc C, Lion L. (2005). Engineered polymericnanoparticles for bioremediation of hydrophobic contaminants.Environ Sci Technol, 39, 1354–8.

Ueji M, Harada M, Kimura Y. (2008). Synthesis of Pt/Ru bimetallicnanoparticles in high-temperature and high-pressure fluids. J ColloidInterface Sci, 322, 358–63.

Vahabi K, Mansoori GA, Karimi S. (2011). Biosynthesis of SilverNanoparticles by Fungus Trichoderma Reesei. Insciences J, 1, 65–79.

Vigneshwaran N, Kathe AA, Varadarajan PV, et al. (2006). Biomimeticsof silver nanoparticles by white rot fungus, Phaenerochaetechrysosporium. Coll Surf B: Biointerf, 53, 55–9.

Wagner V, Dullaart A, Bock AK, Zweck A. (2006). The emergingnanomedicine landscape. Nature Biotechnol, 24, 1211–7.

Wang CB, Zhang WX. (1997). Synthesizing nanoscale iron particles forrapid and complete dechlorination TCE and PEBs. Environ SciTechnol, 31, 2154–6.

Wen L, Lin Z, Gu P, et al. (2009). Extracellular biosynthesis ofmonodispersed gold nanoparticles by a SAM capping route.J Nanopart Res, 11, 279–88.

Wu R, Qu J, He H, Yu Y. (2004). Removal of azo-dye Acid Red B (ARB)by adsorption and catalytic combustion using magnetic CuFe2O4

powder. Appl Catal B, 48, 49–56.Wu R, Qu J. (2005). Removal of water-soluble azo dye by the magnetic

material MnFe2O4. J Chem Technol Biotechnol, 80, 20–7.Xie C, Xu F, Huang X, Dong C, Ren J. (2010). Single gold nanoparticles

counter: an ultrasensitive detection platform for one-step homoge-neous immunoassays and DNA hybridization assays. J Am Chem Soc,131, 12763–70.

Xiu Z, Jin Z, Li T, et al. (2010). Effects of nano-scale zero-valent ironparticles on a mixed culture dechlorinating Trichloroethylene. BioresTechnol, 101, 1141–6.

Xu S, Liu H, Fan Y, et al. (2012). Enhanced performance and mechanismstudy of microbial electrolysis cells using Fe nanoparticle-decoratedanodes. Appl Microbiol Biotechnol, 93, 871–80.

Yan B, Wrenn BA, Basak S, et al. (2008). Microbial reduction of Fe(III).in hematite nanoparticles by Geobacter sulfurreducens. Environ SciTechnol, 42, 6526–31.

Yang HH, Zhang SQ, Chen XL, et al. (2004). Magnetite-containingspherical silica nanoparticles for biocatalysis and bioseparations. AnalChem, 76, 1316–21.

Yang N, Zhu S, Zhang D, Xu S. (2008). Synthesis and properties ofmagnetic Fe3O4-activated carbon nanocomposite particles for dyeremoval. Mater Lett, 62, 645–7.

Yavuz H, Denizli A, Gungunes H, et al. (2006). Biosorption of mercuryon magnetically modified yeast cells. Sep Purif Technol, 52, 253–60.

Yellen BB, Forbes ZG, Halverson DS, et al. (2005). Targeted drugdelivery to magnetic implants for therapeutic applications. J MagnMagn Mater, 293, 647–54.

Yee CK, Jordan R, Ulman A, et al. (1999). Novel one-phase synthesis ofthiol-functionalized gold, palladium, and iridium nanoparticles usingsuperhydride. Langmuir, 15, 3486–91.

Yong P, Rowsen NA, Farr JPG, et al. (2002). Bioreduction andbiocrystallization of palladium by Desulfovibrio desulfuricansNCIMB 8307. Biotechnol Bioeng, 80, 369–79.

Zhang C, Vali H, Romanek CS, et al. (1998). Formation of single-domain magnetite by a thermophilic bacterium. Am Mineral, 83,1409–18.

Zhang H, Li Q, Lu Y, et al. (2005). Biosorption and bioreduction ofdiamine silver complex by Corynebacterium sp. J Chem TechnolBiotechnol, 80, 285–90.

Zhang G, Qu J, Liu H, et al. (2007a). CuFe2O4/activated carboncomposite: A novel magnetic adsorbent for the removal of acid orangeII and catalytic regeneration. Chemosphere, 68, 1058–66.

Zhang G, Qu J, Liu H, et al. (2007b). Preparation and evaluation of anovel Fe–Mn binary oxide adsorbent for effective arsenite removal.Water Res, 41, 1921–8.

Zhang X, He X, Wang K, et al. (2009). Biosynthesis of size-controlledgold nanoparticles using fungus, Penicillium sp. J Nanisci Nanotecnol,9, 5738–44.

Zhang X, Yan S, Tyagi RD, Surampalli RY. (2011). Synthesis ofnanoparticles by microorganisms and their application in enhancingmicrobiological reaction rates. Chemosphere, 82, 489–94.

Zhang T, Kim B, Levard C, et al. (2012). Methylation of mercury bybacteria exposed to dissolved, nanoparticulate, and microparticulatemercuric sulfides. Env Sci Technol, 46, 6950–8.

Zhou L, Gao C, Xu W. (2010). Magnetic dendritic materials forhighly efficient adsorption of dyes and drugs. Appl Mater Interf,2, 1483–91.


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Metallic nanoparticles: microbial synthesis and unique properties for biotechnological applications,...

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